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LONDON--(BUSINESS WIRE)-- Rio Tinto and POSCO, the largest steel producer in South Korea and one of the worlds leading steel producers, have signed a Memorandum of Understanding (MoU) to jointly explore, develop and demonstrate technologies to transition to a low-carbon emission steel value chain. The partnership will explore a range of technologies for decarbonisation across the entire stee

MELBOURNE--(BUSINESS WIRE)-- Rio Tinto has appointed Isabelle Deschamps to succeed Barbara Levi as Chief Legal Officer & External Affairs. Isabelle, who is currently General Counsel of AkzoNobel and a member of the Executive Committee, will join Rio Tinto on 25 October 2021. Isabelle, a dual Canadian and UK citizen, has over 20 years experience in various senior legal roles across Europe

LONDON--(BUSINESS WIRE)-- Rio Tinto has declared force majeure on customer contracts at Richards Bay Minerals (RBM) in South Africa due to an escalation in the security situation at the operations. This has led to the decision to cease operations until the safety and security position improves. Rio Tinto chief executive Minerals, Sinead Kaufman, said: The safety of our people is our top prio

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direct reduction - an overview | sciencedirect topics

Direct reduction of wstite and other forms of iron oxide takes place in the following order. First the reduction of FeO with CO gas (1.1.28), and then the formed CO2 gas reacts with coke generating CO gas again (1.1.27):

Although the total reaction of the direct reduction of wstite is very much thermodynamically in favor with very negative Gibbs energy of reaction, the reaction is highly endothermic, mainly caused by the Boudouard reaction. In reality, most of the unreduced iron in the lower zone is in the form of fayalite (2FeOSiO2) or intermixed in the primary slag. Reduction of FeO in the slag is more difficult than free FeO.

At this high-temperature zone, reduction of wstite by hydrogen can also regarded as direct reduction, since the formed water vapor will react with coke and form H2 and CO, as is shown in reactions (1.1.30) and (1.1.31) [19]:

Two important disadvantages of direct reduction are: (1) excessive consumption of coke and generation of extra CO, which is more than needed in the upper zone of the furnace and (2) excessive energy requirement, which consumes more coke or fuel in the combustion zone. However, the direct reduction guarantees a more complete reduction of iron oxide in the lower zone, which prevents the loss of ferrous materials or their reduction in the hearth of the blast furnace. In practice, it is the combination of indirect reduction in the upper zone and the direct reduction in the lower zone that makes the total reduction of iron oxide an efficient process.

Direct reduction iron or sponge iron is an old method for producing hydrogen (Milne etal., 2006; Pea etal., 2010; Biljetina and Tarman, 1981) that was replaced by more efficient and economic processes. Recently, the interest in sponge iron as a hydrogen production process has grown again, although the technology still has some major technical and economic challenges to overcome (Milne etal., 2006; Pea etal., 2010; Sime etal., 2003). The main reasons for this renaissance are the simplicity of the process and the high purity of the H2 produced (Navarro etal., 2007). The concept is based in a cyclic process. Firstly, Fe oxides are reduced to metallic iron and/or Fe(II) oxide with the syngas (Reactions [xxii] and [xxiii]). The metallic iron is then oxidized to iron oxide using steam (Reaction [xxiv]) (Milne etal., 2006; Pea etal., 2010). Afteroxidation, H2 is recovered and the Fe2O3 is recycled to the initial step (Sime etal., 2003).

Direct reduction of iron ore has been an alternative solution to the BF process to provide the steelmaker the opportunity to utilize raw materials without the need for sintering and cokemaking. Several alternative ironmaking processes have been developed and commercialized such as the HYL, Midrex, ITmk3, FINMET, COREX, and others. More recently, steelmakers have found that a combination of the different processes could be fundamentally utilized to develop new processes that could compete with the productivity and quality of the BF hot metal, but be more economically competitive and environmentally friendly. In particular, the FINEX process, which utilizes iron ore fines and noncoking coals, is one such process that is relatively proven and show significant advantages for those dependent upon imported raw materials, low quality iron ore fines, and noncoking coals.

Driven for the need to maximize the use low quality and low cost raw materials for hot metal production, the FINEX process has significantly advanced from its predecessors of the FINMET (improvement of the FIOR), and COREX process. FINMET (FINos METalizados) uses a series of four fluid bed reactors (R4R3R2R1) with countercurrent gas/solids contacting down the reactor train. Iron ore fines of less than 12mm is charged to the reactor (R4) and preheated to approximately 550C. The reduction of hematite to wustite occurs from reactor R4 to R2. The temperature in R1 is approximately 800C resulting in a final metallization of 93%. To achieve higher metallization with faster reduction kinetics and maintain optimal fluidization of the particles, the FINMET process operates at a pressure as high as 12bars, which causes significant equipment and process-related issues for long-term operations and currently the only plant in operation is the 1million tons Orinico Iron in Venezuela. COREX (COal REduction) uses noncoking coals, which is charged into the meltergasifier producing heat and reducing gases of CO and H2. However, lump ore, sinter, pellets or a mixture of these in the size range of 620mm are reduced in a reduction shaft, unlike the fine iron ores and fluidized bed used in the FINEX process, producing sponge DRI with a metallization of approximately 93%. The as-formed DRI is conveyed into the meltergasifier, where additional reduction and carbon dissolution occurs. The hot metal is separated from the slag and tapped similar to the BF.

Since 1992, POSCO has partnered with Siemens-VAI undertaking R&D activities to develop the FINEX process shown in Figure 4.5.72. The process utilizes nonagglomerated iron ore fines in the range of 0.018mm and noncoking coals briquetted to approximately 50mm. The iron ore fines are reduced in a multistage fluidized-bed reactor (FINMET) and the coal briquettes are charged directly into a meltergasifier (COREX), where it is oxidized by oxygen forming a reducing gas for the fluidized bed. Details of the process are provided in the following section.

As of 2012, two FINEX plants are in operation at Pohang works POSCO. The first is a demonstration plant with an annual capacity of 0.6million tons operating since 2003, which was modified from the original 0.6million tons COREX plant that operated from 1995. The second is a commercial size 1.5million tons of annual capacity operating since 2007 with at least 300 days of continuous operations. A third FINEX plant with an annual capacity of 2.0million tons is under construction and targeted for start-up at the end of 2013.

Metal oxides are most often reduced by carbon or hydrogen. The reason why reduction by carbon is treated in this section on gassolid reaction is because the actual reduction is largely effected by carbon monoxide gas generated by the reaction of carbon dioxide with carbon, when carbon is used to reduce metal oxides in solid state. These reactions can in general be expressed as follows:

The amount y, which is determined by the pCO2/ pCO ratio in the product gas mixture, depends on the kinetics and thermodynamics of the two gassolid reactions (1.1) and (1.2). In many systems of practical importance, reaction (1.1) is much faster than reaction (1.2), and thus the pCO2/ pCO ratio approaches the equilibrium value for reaction (1.1). The overall rate of reaction (1.3) is then controlled by the rate of reaction (1.2) taking place under this pCO2/ pCO ratio (Padilla and Sohn, 1979).

The reduction of iron oxide is the most important reaction in metal production, because iron is the most widely used metal and it occurs in nature predominantly as hematite (Fe2O3). The production of iron occupies more than 90% of the tonnage of all metals produced. The most important reactor for iron oxide is the blast furnace, in the shaft region of which hematite undergoes sequential reduction reactions by carbon monoxide (Table 1.1).

In the blast furnace, the solid charge flows downward, and the tuyere gas with a high CO/CO2 ratio flows upward. Thus, the tuyere gas first comes into contact with wustite (FeO), the reduction of which requires a high CO/CO2 ratio, as seen above. The resulting gas reduces magnetite (Fe3O4) and hematite (Fe2O3) on its way to the exit at the top of the furnace.

The equilibrium percentage of CO in a mixture with CO2 is shown in Fig.1.1 as a function of temperature. Again, it is seen that the equilibrium concentration of CO for the reduction of hematite to magnetite is essentially zero; i.e., CO is completely utilized for the reduction. The equilibrium content of CO for the reduction of Fe3O4 to FeO and that of FeO to Fe depend on temperature. It is also noted that wustite is a non-stoichiometric compound FexO with an average value of x equal to 0.95 in the temperature range (approximately 600C 1400C) of its stability. The actual value of x and thus oxygen content depend on temperature and CO/CO2 ratio, as illustrated by the curves drawn within the wustite region in Fig.1.1. Furthermore, the CO/CO2 ratio is limited by the Boudouard reaction given by (eqn 1.2) and shown as a sigmoidal curve in Fig.1.1 (for 1atm total pressure without any inert gas). Thus, the reduction reactions indicated by the dashed lines to the left of this curve are thermodynamically not feasible. (In practice, however, reduction by CO to the left of the Boudouard curve is possible because the carbon deposition reaction (the decomposition of CO) to produce solid carbon is slow.)

The reduction of iron oxide by hydrogen is important in the production of direct reduced iron. This method of iron production is gaining increasing significance as an alternative route to the blast furnace technology with the many difficult issues facing the latter, the most important being the problems related to environmental pollution and the shear size of the blast furnace. Direct reduction technology for iron encompasses the processes that convert iron oxides into metallic iron in solid state without going through a molten phase. In this technology, iron-bearing materials are reduced by reacting with reducing substances, mainly natural gas or a coal, at high temperatures but below the melting point of iron. The product, direct reduced iron (DRI), is a porous solid, also known as sponge iron. It consists primarily of metallic iron with some unreduced iron oxides, carbon and gangue. Carbon is present in the range of 14%. The gangue, which is the undesirable material present in the ore, is not removed during reduction as no melting and refining take place during the reduction process. The main usage of DRI products is in the electric arc furnace (EAF). However, due to its superior characteristics, DRI products have found their way into other processes such as blast furnaces, basic oxygen furnaces and foundries. Globally, DRI comprises about 13% of the charge to the EAF (Kopfle et al., 2001). Nowadays, the percentage of crude steel produced by BOF is approximately 63%, while that of EAF is about 33%, and the balance 4% is made up of the open hearth (OH) steel (International Iron and Steel Institute, 2004). However, the contribution of EAF to the world crude steel output is expected to increase to reach 40% in 2010 (Gupta, 1999) and 50% in 2020 (Bates and Muir, 2000).

There have been major developments in direct reduction processes to cope with the increasing demand of DRI. DRI production has increased rapidly from 0.80 million tons per year in 1970 to 18 million tons in 1990, 44 million tons in 2000, and 49 million tons in 2003 (MIDREX, 2004). The worldwide DRI production is expected to increase by 3 Mt/y for the period 20002010 (Kopfle et al., 2001).

Reduction of iron bearing materials can be achieved with either a solid or gaseous reductant. Hydrogen and carbon monoxide are the main reducing gases used in the direct reduction (DR) technology. These gases are largely generated by the reforming of natural gas or the gasification of coke/coal. In reforming, natural gas is reacted with carbon dioxide and/or steam. The product of reforming is mainly H2 and CO, whereas CO is the main product from coal gasification. Reduction reactions by reducing gases take place at temperatures in the range of 850C1100C, whereas those by solid carbon occur at relatively higher temperatures of 1300C1500C. Carburization reactions, on the other hand, take place at relatively lower temperatures below 750C. For reforming reactions, the reformed gas temperature may reach 950C for the stoichiometric reformer, and 780C in the case of a steam reformer.

Direct reduction (DR) processes have been in existence for several decades. The evolution of direct reduction technology to its present status has included more than 100 different DR process concepts, many of which have only been operated experimentally. Most were found to be economically or technically unfavorable and abandoned. However, several were successful and subsequently improved to develop into full-scale commercial operations. In some instances, the best features from different processes were combined to develop improved processes to eventually supplant the older ones.

Direct reduction processes may be classified, according to the type of the reducing agent used, to gas-based and coal-based processes. In 2000, DRI produced from the gas-based processes accounted for 93%, while the coal-based processes produced 7%. Gas-based processes have shaft furnaces for reducing. These furnaces can be either a moving bed or a fluidized bed. The two most dominant gas-based processes are MIDREX and HYL III, which combined to produce approximately 91% of the worlds DRI production. Fluid-bed processes, by contrast, have recently received attention, because of its ability to process fine iron ores. These processes are based either on natural gas or coal. A list of the processes together with their relevant characteristics is given in Table 1.2 (MIDREX, 2001).

The gaseous (or carbothermic) reduction of nickel oxide, obtained by dead roasting of nickel sulfide matte or concentrate, is an important intermediate step for nickel production. In the Mond process, crude nickel is obtained this way before undergoing refining by carbonylation. Crude nickel has sometimes been cast into anodes and electrolytically refined. Nickel laterite ores are reduced by carbon monoxide before an ammoniacal leach. Nickel oxide reduction reactions are simple one-step reactions, as follows:

Both reactions have negative Gibbs free energy values. For hydrogen reduction it is 7.2 and 10.3kcal/mol, respectively, at 600K and 1000K. For reduction by CO, the free energy values are 11.1kcal/mol at both 600K and 1000K. The thermodynamic data used here as well as below were obtained from Pankratz et al. (1984). The corresponding equilibrium ratio pH2/pH2O is 2.4103 and 5.6103, respectively, at 600K and 1000K, and the equilibrium ratio pCO2/pCO is 9.5105 and 3.7103, respectively, at the same temperatures. Therefore, the reactant gases are essentially completely consumed at equilibrium in both cases. These reduction reactions are mildly exothermic, the standard enthalpy of reaction (Hro) being 2 to 3kcal/mol for hydrogen reduction and 11.2 to 11.4kcal/mol for reduction by carbon monoxide.

Zinc occurs in nature predominantly as sphalerite (ZnS). The ZnS concentrate is typically roasted to zinc oxide (ZnO), before the latter is reduced to produce zinc metal by the following reactions (Hong et al., 2003):

The overall reaction is essentially irreversible (G=12.2kcal/mol at 1400K) and highly endothermic (H=+84.2kcal/mol at 1400K) and the gaseous product contains a very small amount of CO2 at temperatures above 1200K (Hong et al., 2003). It is also noted that this reaction is carried out above the boiling point of zinc (1180K), and thus zinc is produced as a vapor mixed with CO and the small amount of CO2 from the reaction. Zinc is recovered by condensation. Zinc vapor is readily oxidized by CO2 or H2O (produced when coal is used as the reducing agent) at lower temperatures. Thus, zinc condensation should be done as rapidly as possible, and the CO/CO2 ratio in the product gas must be kept as high as possible by the use of excess carbon in the reactor.

The final process in tungsten production is the hydrogen reduction of the intermediate tungsten oxide (WO3 or W4O11) obtained through the various processes for treating tungsten ores. Because of the substantial volatility of the higher oxide, its reduction is carried out at a low temperature to obtain nonvolatile WO2. WO2 is then reduced to tungsten metal at a higher temperature (Habashi, 1986), as indicated below:

The reduction reaction is carried out at about 2200C and thus magnesium is produced as a vapor (B.P. = 1090C). Much like zinc vapor mentioned earlier, magnesium vapor is susceptible to oxidation and requires similar measures for its condensation and collection.

For other aspects of gaseous reduction of metal oxides, including reduction by carbon involving gaseous intermediates, the reader is referred to the literature (Alcock, 1976; Evans and Koo, 1979; Habashi, 1986).

Smelting and direct reduction technologies are being typically indicated as alternatives to the BF; in the future, these processes might be complementary. For example, a process scheme for HRG injection based on the coupling of Corex and BF was suggested (Figure 17.31). In this technology, the Corex export gas after the removing of CO2 is heated up and then injected into the BF (Wiesinger et al., 2001).

Looking at direct reduction processes, not only off-gases but also sponge iron in form of DRI or LRI might be used in the BF. Figure 17.32 shows a proposed and tested laboratory-scale operation modus of the Circofer process (a coal-based direct reduction process using a CFBcirculating fluidized bed reactor), in which products DRI/LRI and char are used in the BF, for example, by means of injection via tuyeres (Born et al., 2012).

Because the direct reduction of iron is a solid-state process, the product DRI has roughly the same size and shape as the starting particles, whether roughly spherical pellets or irregularly shaped lumps. Due to process kinetics and the overall economics of direct reduction, very few DRI particles actually approach 100% metallization; metallizations in the best plants in 2012 were around 96%. In addition, as discussed above, there is carbon pickup as well, with the final product containing between 0.5% and 4% carbon. This is mostly present as iron carbide, though some free carbon can be found. DRI with constant metallization and carbon content can be produced reproducibly in a given plant with a given feed and operating conditions; this is a one great advantage to customers compared to even the best scrapuniform physical and chemical properties.

However, given metallization rates of 9095% and the concomitant oxygen removal, DRI particles are extremely porous, and given the omnipresence of oxygen in the atmosphere, there is always the struggle to minimize reoxidation of the reduced iron. This is made more difficult by that porous nature, resulting in internal surface areas several thousand times greater than the external area of the pellet or lump. Since individual pellets, and a large bed of pellets, are poor thermal conductors, and iron oxidation is exothermic, it is possible for large concentrations of DRI (such as in a storage pile or the hold of a ship) to oxidize in the presence of air or water and heat up. In the worst case, the temperature becomes high enough to reduce water, releasing hydrogen, which can explode in a confined space. This has happened often enough that shipping of DRI is heavily regulated by the International Maritime Organization (IMO).

In subsequent sections, the causes of DRI overheating are discussed in more detail, followed by some of the history of transportation and shipping of DRI, and finally measures to reduce the reactivity of DRI, particularly passivation and conversion of DRI to HBI.

In the cement, DRI and fertiliser industries, it is becoming economically more attractive to have captive jig-based washeries in conjunction with fluidised bed power plants. This tends to promote lower cost, jig-based washing and to create a barrier for the more expensive Dense Media Cyclone (DMC) washing. Dry jigging plants are becoming more widely used to remove some of the obvious stones, and the product obtained from de-stoning is often combined with some coal washery reject and dust collector fines to produce a power plant feed. The generation cost with such a feed varies from Rs 1.003.50 per unit (kWh), with the upper limit being for the plants operating in isolation mode and at a low plant load factor (PLF). The cost range nevertheless is very competitive compared to non-coal technologies and at times significantly less than the industrial power tariff. One of major Indian cement industries (ACC) pays an average of Rs 4.86 per unit for grid power while its coal based captive power plant average generation cost is Rs 3.72 per unit. Captive washeries (those supplying directly to a user) of virtually all the cement producing plants are now jig based.

The first tap of pig iron produced via a direct reduction technology developed in Brazil took place in September 2011. This was in the Tecnored demonstration plant located in Pindamonhangaba, Sao Paulo State which has a 75 000 tpy production capacity. This is the result of a 35-year technological effort by universities and the industry to study the pros and cons of the technology and its scale-up development. The Catholic University of Rio de Janeiro (PUC-RJ) kicked off with initial studies in 1974. In 2009, Vale acquired equity majority with 43.04%; Brazilian Development Bank (BNDES) entered with 31.79% while developers known as Logos Tecnocom kept 25.17%, forming the joint venture Tecnored Desenvolvimento Tecnologico S/A (Vale, 2011; ABM Metalurgia, 2011).

A total investment of R$ 250 million has already been made by JV partners. Future plans are to ensure operational stability and to study the economic feasibility of expanding to a bigger plant of 300 kt per annum.

Oxygen is a convenient oxidant; however, its direct reduction on the majority of electrode materials requires substantial overpotential.3537 One of the solution for this problem is to modify the cathodes with enzymes, for example, BOD, catalyzing reduction of oxygen to water. BOD from M.verrucaria is the most extensively studied BOD for construction of BFC cathodes; however, BOD from other sources have also been evaluated (Table1). As shown in Table1, the formal potential of the T1 copper site of these BOD are relatively close to the thermodynamic potential of oxygen reduction to water. The simplest construction of BOD-based cathode is obtained by physical adsorption of the enzyme on the surface of the electrode. It has been demonstrated that rational modification of the surface to either mimics the substrate (bilirubin)47,48 or creates charge complementarity to the T1 copper region of a particular BOD, ensures correct enzyme orientation enabling facile DET coupling of the enzyme.49 In general, better DET coupling of M.verrucaria BOD is obtained on negatively charged surfaces.47,5052 Additionally, high-surface area of nanomaterial modified electrodes allows adsorption of high amount of BOD making electrodes considerably more stable.53,54 3D AuNP-modified electrodes impregnated with BOD were shown to be stable over a couple of days under operation in buffer solution.55 High amount of the BOD at the cathodes can also be secured by their wiring with osmium-based redox polymers.35,5659

Silicothermic reduction is the most commonly employed production process for the direct reduction of MgO. The most important equipment for this process is the retort-type reduction furnace. Numerous furnaces that encompass various designs for components such as reaction vessels and condensers have been proposed. Among these, the most representative method is the Pidgeon process.

Figure 2.9.40 shows the production process of magnesium by the Pidgeon process. MgOCaO is produced by calcining dolomite. The calcined material is mixed and briquetted with ferrosilicon (typically 7580% Si) at a molar ratio of MgO:Si=1.25:1 and then charged in retorts as shown in Figure 2.9.41. The retort is comprised of a thick heat-resistant steel (NiCr steel). A large number of pellets are placed in the horizontal retort. The retort is then heated from the outside by gas burners or resistance heaters. The retort is kept at 1150C for 810h under about 102mmHg. The following reactions take place:

Magnesium vapor formed by the reduction transfers through gas phase and condenses on a low-temperature region of the retort. About 20kg of magnesium metal is produced per 120130kg of pellets, which indicates that the yield of the reaction is about 85%. The collected condensed Mg is remelted and cast into a mold to form an ingot. The purity of the magnesium metal is 99.95%.

sewage sludge coke estimation using thermal analysis | springerlink

The imposition of more stringent legislation by CETESB in the State of So Paulo (Brazil) governing the disposal and utilization of sewage sludge, coupled with the growth in its generation has prompted a drive for alternative uses of sewage sludge. One option that is especially promising, due to its potential to valorize sludge, is its conversion into carbonaceous adsorbents or coke for industrial effluents treatment. Thus, a methodology is presented to estimate the coke produced from the sludge of a sewage treatment station using thermal analysis. The used sewage sludge, which comes from aerobic treatment, was collected in the wastewater treatment station of Barueri, one of the largest of the So Paulo metropolitan area. The sludge samples were collected, dried, ground, and milled until they passed an ABNT 200 sieve. The inert ambient used during its thermal treatment produces inorganic matter and coke as residual materials. Coke formation occurs in the 200500C range and, between 500 and 900C, its thermal decomposition occurs. The highest formation of coke occurs at 500C.

Mocelin C. Sewage sludge pyrolysis: Production of adsorbent and fuel oils, MSc Dissertation-Post-graduate in Mechanical Engineering and Materials, Federal Technological University of Parana, Curitiba, Brazil, 2007.

Ischia M, Maschio R, Grigiante M, Baratieri M. Clay-sewage sludge co-pyrolysis. A TG-MS study on potential advantages afforded by the presence of clay in the pyrolysis of wastewater sewage sludge. Waste Manag. 2011;31:717.

Samtani M, Dollimore D, Alexander KS. Comparison of dolomite decomposition kinetics with related carbonates and the effect of procedural variables on its kinetic parameters. Therm Acta. 2002;392393:13545.

The authors wish to thank CAPES (Coordination for the Improvement of Higher Education), FAPESP (the State of So Paulo Research Foundation), and CNPq (Brazilian National Council of Scientific and Technological Development) for the financial support.

Viana, M.M., Melchert, M.B.M., de Morais, L.C. et al. Sewage sludge coke estimation using thermal analysis. J Therm Anal Calorim 106, 437443 (2011). https://doi.org/10.1007/s10973-011-1392-1

global management consulting firm | bain & company

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insight on thermal stability of magnetite magnetosomes: implications for the fossil record and biotechnology | scientific reports

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Magnetosomes are intracellular magnetic nanocrystals composed of magnetite (Fe3O4) or greigite (Fe3S4), enveloped by a lipid bilayer membrane, produced by magnetotacticbacteria. Because of the stability of these structures in certain environments after cell death and lysis, magnetosome magnetite crystals contribute to the magnetization of sediments as well as providing a fossil record of ancient microbial ecosystems. The persistence or changes of the chemical and magnetic features of magnetosomes under certain conditions in different environments are important factors in biotechnology and paleomagnetism. Here we evaluated the thermal stability of magnetosomes in a temperature range between 150 and 500C subjected to oxidizing conditions by using in situ scanning transmission electron microscopy. Results showed that magnetosomes are stable and structurally and chemically unaffected at temperatures up to 300C. Interestingly, the membrane of magnetosomes was still observable after heating the samples to 300C. When heated between 300C and 500C cavity formation in the crystals was observed most probably associated to the partial transformation of magnetite into maghemite due to the Kirkendall effect at the nanoscale. This study provides some insight into the stability of magnetosomes in specific environments over geological periods and offers novel tools to investigate biogenic nanomaterials.

Magnetosomes are intracellular single domainnanocrystals of magnetite (Fe3O4) or greigite (Fe3S4) enveloped by a lipid bilayer. These structures are produced by magnetotactic bacteria through a genetically controlled biomineralizationprocess1. Besides havingcontrol over the chemical composition, magnetic properties, shape and size of magnetosome crystals, magnetotactic bacteria also have a cytoskeletal-like structure along which magnetosomes are organized in single or multiple chains, imparting to the cell a magnetic moment and the ability to passively orient along magnetic field lines, in particular the Earths geomagnetic field2. Currently magnetotactic bacteria are affiliatedto several groups in the domain Bacteria and may have existed since the Archean Eon3. The ecological importance of this apparently ancient trait is to assist bacterial chemotaxis in more efficiently locating an optimal position in vertical chemical gradients forsurvival using the geomagnetic field1,3.

Specific properties of magnetosome magnetite crystals have long been used to differentiate fossilized remains of magnetotactic bacteria (magnetofossils) in sediments and rocks from magnetites of inorganic origin4. In some cases, magnetofossilsappear to remain preserved for millions of years5. The resistance of magnetofossils to diagenesis and extreme environmental changes has been described in some detail6. Thus, these nanoparticles may provide an important record of ancient ecosystems.

Several techniques are used to determine the presence of biogenic magnetite in sediment6,7,8. These include characterizations of crystal sizes and shape distributions, crystal morphologies, arrangement, chemical purity, and crystallographic perfection determined using high-resolution transmission electron microscopy (HRTEM), off axis electron holography and nanometer scale chemical analysis9,10,11. To our knowledge, a real-time analysis of the thermal stability of magnetite magnetosomes in an oxidative environment has never been performed. This information is essential in understanding magnetofossil stability in the environment and in any prediction of modification of their crystalline structure over geological time scales and extreme conditions.

Characterization of the thermal stability of magnetosomes under oxidizing conditions is also relevant from a technological point of view. The unique properties of magnetosomes described above, especially the presence of an external lipid bilayer with associated proteins, place them in the spotlight as tools in the next generation technologies12. In nanomedicine, for example, magnetite magnetosomes have proven to be efficient tools in the development of both drug delivery systems and in magnetic fluid hyperthermia13,14. Enzymatic nanocomplexes for industrial applications have also been developed using magnetite magnetosomes. In these cases, enzymes can be attached to the surface of magnetosomes to concentrate or eliminate target molecules15,16. For both biomedical and industrial applications, the magnetic properties, as well as morphological and structural features of magnetosomes, should be maintained during the treatment period or as much as possible for reuse of enzymatic complexes, respectively. So far, the studies reporting the modification of magnetite magnetosomesproperties whensubjected to thermal treatments were only performed under relatively moderate temperatures, which are relevant for biomedical applications that usually reach values below 50C;in this general framework, it is worthy to note that a nanometer-scale characterization of the modifications of these structures induced by a heat induction process was not reported until now17.

Several studies have shown that inorganic magnetite is transformed into maghemiteat moderate temperatures (below 250C) under an air atmosphere18,19,20,21. Here we subjected elongated prismatic magnetite magnetosomes to temperatures ranging from 150 to 500C under O2 at atmospheric pressure and analysed the shape, oxidation state variation and crystallographic structure of the magnetosomes by high-resolution, tomographic and analytical electron microscopy techniques.

Conventional transmission electron microscopy (CTEM)images of the purified magnetite magnetosomes of Magnetovibrioblakemoreistrain MV-1 showed the presence of the magnetosome membrane, which envelops each crystal (Fig.1A). Deposition of the magnetosomeson the in situE-chip was checked and the areas for study were selected (Fig.1B; circles). For real-time thermal stability evaluation of magnetosomes, the sample was heated to 150C under an Ar atmosphere for 1h and no changes were observed in the magnetite crystal or magnetosome membrane (Fig.1C; arrow).The magnetosome membrane became more apparent upon the injection of O2 in the in situ chamber and increasing the temperature to 300C. The continuous temperature increase (150300C) also affected the smooth appearance of the magnetosomes membrane, which became more irregular and rough, suggesting an aggregation of lipids and denaturation of proteins (Fig.1D-F, arrows).The comparison of the crystalline structure of magnetosomes before and after being subjected to heat and an oxidizing atmosphere showed no changes in the mineral component of the magnetosomes. Although ultrastructural changes were observed on the magnetosome membrane after heating the sample to 300C under oxidizing conditions (Fig.1CG), in order to obtain a better evaluation of the membrane transformation, observations of the same field were made at room temperature without the upper nitride silicon window of the holders chamber(Fig.2), which allows obtaining images of better resolutions, unaffected by the interactions of the electrons with the upper membrane and the oxygen present in the Protochips cell.

Evaluation of the thermostability of magnetite magnetosomes by bright field scanning transmission electron microscopy (BF-STEM). (A) Purified magnetosomes showing the presence of the surrounding membrane (arrow). (B) Low magnification image of the E-chip used for the environmental gas STEM analysis (asterisk) showing the analysed areas in the electron transparent wheel of the E-chip device(circles). The black circle shows the region exhibited at higher magnification in (C-F) where the same magnetosomes subjected to different conditions are shown. White circles correspond to areas used in other analysis. (C) Magnetosomes subjected to 150C for 1h under an argon (Ar) atmosphere. (D) Magnetosomes subjected to 150C for 1h under an O2 atmosphere. (E) Magnetosomes subjected to 200C for 1h under an O2 atmosphere. (F) Magnetosomes subjected to 300C for 1h under an O2 atmosphere. (G) High-resolution-TEM image of the same magnetosomeafter 300C exposed to O2, showing the crystal structure without alteration and the presence of a membrane (arrows). The arrows in (C-F) were included for comparison of the thicknesses of the magnetosome membranes. Images show that membranes are apparent in (D-F) and present a non-uniform aspect like exfoliation around the magnetite crystal (arrows). Scale bar in (F) applies to (C-E).

BF-STEM images before and after oxidation treatment at 300C.Observation made at room temperature, without the upper membrane which closes the E-Chip containing the sample. This greatly increase the signal-to-noiseratio in the image, due to the absence of theinteraction of the electrons with silicon nitride cover andwith gaseous oxygen atoms. (A,D) Before oxidation treatment, the initial thickness of the membrane is of about 2.6nm. (B,C) After oxidation treatment, the thickness of the membrane is reduced(arrows in B). (E,F) show details of thethickness (E) and of the structure (arrows in F) of the membrane after treatment.

High-resolution bright-field scanning transmission electron microscopy (BF-STEM) observation after cooling showed the presence of the membrane around the magnetite crystals (Fig.2), suggesting that the bilayer deforms and undergoes organizational changes after heating. Comparison of the structure of the membrane before (Fig.2A,D, Supplementary Fig.S1) and after oxidation (Fig.2B,C,E,F), clearly shows that the structure formed in the course of the oxidation, which surrounds it under the appearance of a hair or plum, does not seem to have affected its original morphology. Its thickness is reduced as shown by the comparison between the images in Fig.2D,E, but entirely envelopes the crystals.

Energy-dispersive X-ray spectroscopy (EDS) line scan analysis after sample heating and cooling corroborated this result by detecting phosphorus across the magnetosome (Fig.3A,B). Interestingly, high amount of iron is only detected until the edge of the magnetosome crystal and not in the regions surrounding the crystals, suggesting that the magnetite crystals were not degraded during the increase in temperature and exposure to O2. However, in the analysis approach using STEM tomography before and after oxidation (Fig.4 and Supplementary Fig.S2), nanopores formed at the interfaces between the magnetite nanocrystals and the presence of a significant roughness of the outer faces of the crystals were observed after treatment (Fig.4E,F).

High-resolution STEM images and energy-dispersive X-ray spectroscopy (EDS) line scan microanalysis of magnetosomes heated to 300C. (A) HAADF image of isolated magnetosomes showing the EDS line scan region (blue line; pink dots represent areas corresponding to measurements displayed in (B); the white arrow represents the direction of scanning); (B) Line scan results showing that phosphorus is detected over the entire crystal, and this signal increases close the facets (red rectangles, because the electron beam passes through a larger thickness of membrane, in fact the beam close to the edges has a parallel direction to the membrane. Note that minor amount of iron is detected outside the magnetosome (at the LG30000 and LG30009 positions). A small signal of Fe could orginate from the polepieceof the microscope, as related by Williams and Carter28.

STEM image and tomography slices of a magnetosome chain before and after oxidation at 300C. Before: (A) BF-STEM image. Tomography performed in HAADF-STEM mode from 55.5 to +55.5 with astep of 1.5and acquisition magnificationof 800.000X. (B,C) Slices extracted from the reconstructed volume at two different depths. After: (D) BF-STEM image. Tomography performed in the same conditions as previously. (E) and (F) Slices extracted from the reconstructed volume at two different depths. The dotted ellipses in redsurround nanopores formed at the interfaces between magnetite nanocrystals. The arrows point to the presence of a significant roughness atthe external faces of the magnetosome.

When magnetosomes were heated until 500C significant alterations of the magnetite crystalswere observed (Fig.5). Although in CTEM magnetosomes seemed completely damaged (Fig.5C), in the non-irradiated regions illustrated inFig.5D,E the general morphology of the crystals was preserved. However, a hollow structure, similar to a cavity, appears in the magnetosomes. Similar structures were observed in the experiment with the microscope operating in STEM mode (Fig.6A,C). Semi quantitative analysis of the damaged areas of theses magnetosomes by ELNES (energy loss near edge structure) of oxygen (O-K edge around 540eV) and iron (Fe-L edge around 710eV) indicated modifications in their chemical composition (Fig.6). Bright areas in the HAADF images of Fig.6 represent the unaffected portion of magnetosomes, while dark areas are cavities that presented significant iron loss and unbalance proportion of oxygen in relation to magnetite, showing a change in the mineral phase (Fig.6B,D). The presence of iron oxides was not detected in the area around the magnetosome in these samples, byusing EELS (see also Supplementary Fig.S4).

CTEM images of magnetosomes during in situ heating experiment when subjected to 150C until 500C and exposed to Ar and O2. From (A) to (C) in irradiation condition, (A) CTEMimage of a chain of magnetosomes at 150C with Ar; (B) CTEMimage of the same chain shown in (A) after heating to 300C and exposed to O2; (C) CTEMimage of the same chain shown in (B) after heating to 500C and exposed to O2and irradiated by the electron beam; (D) CTEMimage of magnetosomes at 500C exposed to O2 obtained in a region that has not been irradiated by the electron beam. Note that the general shape of the magnetosome is maintained, but cavities occur in some crystals. (E) Enlarged image of the boxed area in Fig. D (see also the supplementary Fig.S3) showing a cavity in the magnetosome structure. Inset shows the FFT corresponding to this high-resolution image. The corresponding zone axis can be assigned to magnetite or maghemite but also to a mixed structure (see also Supplementary Fig.S5).

HAADF-STEM images and EELS microanalysis of magnetosomes after heating until 500C and exposure to O2, showing the irregular contrast on magnetosomes and the presence of large cavities. (A) HAADF-STEM image of magnetosomes with cavities. Non-altered regions represented by the red line segment (number 1) and a cavity indicated by the black line segment (number 2) were selected for EELS analysis showed in (B); (B) EELS spectra and relative quantification of regions indicated by red line 1 and black line 2 in (A) for oxygen 540eV and iron 710eV; (C) HAADF-STEM image of magnetosomes with cavities. Non-altered regions represented by the red line (number 1) and a cavity indicated by the black line (number 2) were selected for EELS analysis showed in (D); (D) EELS spectra and relative quantification of regions indicated by red line segment 1 and black line segment 2 in (C) for oxygen 540eV and iron 710eV.

Based on our CTEM, BF-STEM high-angle annular dark field (HAADF-STEM) mode, EDS and electron energy loss spectroscopy (EELS) results, magnetosomes are thermostable nanoparticles when subjected to temperatures upto 300C. It is difficult to clearly visualize the morphology of the membrane from a direct analysis of the images (Fig.1) obtained at different temperatures 150C, 200C and 300C. Indeed, in the environmental TEM mode, the images of the magnetosomes are obtained by collecting the transmitted electron beam which cross also the double SiN membrane (i.e., the top and bottom chips which isolate the environmental cell) and that degrades the contrast of the images due to the additional diffusion contribution; however, it is possible to distinguish some changes at 200C and 300C which are highlighted by arrows in Fig.1E,F. These changes can be better visualized after the return to the room temperature and the removal of the sealing cover (Fig.2). Using these specific observation conditions, some details of the microstructure of the sample after treatment can be clearly observed, particularly the fact that the general appearance of the structure can be assigned to a hair or plume which seems to originate from the membrane and the surrounding part of the magnetosome (Fig.2B,C,E,F). From a quantitative point of view, though the membrane keeps its initial appearance, its thickness goes from a value of about 2.6nm to values between 2.1 and 2.4nm.

The membrane of magnetosomes is a lipid bilayer functionalized by specific proteins involved in the synthesis of magnetosome. Most of the membrane lipids exist in the lamellar or bilayer phase, in particular in a lamellar liquid crystalline phase but sometimes in the lamellar gel phase22. Until now we were not able to specifically determine the structure and physical properties of lipid bilayer membranes of magnetosomes. However, it is generally admitted that lipid bilayer membranes may exhibit, in some cases, a typical behavior specific to a gel or to a liquid, depending on the temperature. It should be thus assumed that, with the rise in temperature, the magnetosome membrane passes through a liquid state which leads to the segregation of the proteins on their surface. This state is a posteriori visible in the electron microscopy images through the formation of plumes associated to a subsequent decrease of the thickness. However, it is important to note that the general morphology and the global localization of membranes around the crystals are preserved during the thermal treatment.

In nature, the oxidation of magnetite to maghemite is probably the most common oxide mineral alteration. This reaction invariably takes place in fine particles after exposure to air at room temperature. The oxidation of magnetite to maghemite at temperatures close to 200C was reported when the magnetite is well ordered and free of stacking faults, whereas magnetite containing stacking faults oxidizes partially to -Fe2O3and lowered the transformation of magnetite to hematite19,20,21. As shown in the high-resolution image (Fig.1G) the magnetite crystalline structure was conserved at the subnanometric scale when samples were subjected to 300C in the presence of O2. No defects were visible (phase transformation corrosion recrystallization or dislocations) and the perfection of the crystalline structure characteristic of biogenic magnetite, was preserved.The STEM mode can be considered to a certain extent as a method of chemical analysis because the contrast of the images variesroughly as the square of the mass of the studied sample, being thus sensitive to its thickness and to the mass of the atoms present in the sample23. Combined with tomography, this technique allows a three-dimensional view of the nanocrystals with a qualitative analytical selectivity. The extracted sections are the result of a deconvolution and reconstruction process of hundreds of images and consequently the signal-to-noise ratio in the sections extracted from the tomograms is considerably improved as compared to classical 2D images; in addition, this slice by slice analysis allows for a fine analysis of the contrast which highlights now only variations in atomic mass and not in thickness, facilitating thus the interpretation of the images in terms of spatial distributions of the chemical elements present in the specimen24. Electron tomography is the most appropriate technique for evaluating porosity characteristics at the nanoscale25. Applied to our specimens in their initial state, it shows that the crystal facets are quite regular and that the magnetosomesdo not contain a nanoscale porosity inside, as shown by the typical slices extracted from the reconstructed volume (Fig.4AC). On the other hand, after the oxidation at 300C, the tomography results (Fig.4D,E,F) show that the core of the crystals has not been modified; the corresponding volume is homogeneous and without porosity.

This result suggests that the magnetosome membrane prevents or slows down the O2 diffusion and thus protects the integrity of the stoichiometry and the structure of the magnetite at temperatures up to 300C.

Interestingly, high-resolution X-ray diffraction of magnetosomes and abiotic magnetite with similar size as magnetosomes has shown that biogenic nanomagnetite is stoichiometric26. The chemical removal of the magnetosome membrane in this study leads to the oxidation of magnetite, revealing the protective character of this biological membrane from oxidation26. To our knowledge, there is no detailed study that has characterized the biochemical properties associated with the protective effect of the magnetosome membrane against oxidation.

Severe damage or transformation was observed on the crystalline structure of the magnetite crystal and the membrane of magnetosomes when samples were heated to temperatures above 300C. Two typical areas on the E-chip containing magnetosomes were analysed. One of the areas has been continuously irradiated by the electron beam during the oxygen treatment (Fig.5AC); a clear morphological transformation of the irradiated magnetosomes can be observed which leads to aggregated amorphous chains at the end of the treatment. This combination of electron beam irradiation and heating effects to transform nanomaterials have been used to create nanoreactors in the field of the development of new nanometric structures27. The other areas of the E-chip containing magnetosome structures that were not irradiated during the heating process under oxidizing conditions (Fig.5A,B) were observed in the low dose mode by reducing the dwell time and the spot size in STEM mode and adjusting the image focus and the electron dose in CTEM mode in a region far from the analysed area. This method is commonly used to study materials sensitive to radiation damage, as for instance biological materials and certain oxides28. In these conditions, by comparing the final morphologies from the two types of areas, continuously irradiated and irradiated only during the data acquisition in the low dose mode, we may unambiguously consider that the morphological and crystallographic transformations of the magnetite nanocrystals, characterized by the formation of hollow structures within the nanocrystals, is exclusively due to an oxidation process whose kinetics depends on the temperature and the speed of cation diffusion18.

In conclusion, as can be seen in Fig.5C, when a region is observed continuously under irradiation, significant damage occurs, in particular, the aggregation of nanocrystals in the form of clusters. Therefore, damages observed in the non-irradiated crystals, which are represented by hollow structures or cavities, likely resulted from vacancy effect rather than damage from the electron beam. It is difficult to distinguish magnetite from the maghemite by electron diffraction and even by FFT of the high-resolution images (Supplementary Fig.S3). Indeed magnetite presents a mixed-valence given by the presence ofFe2+, Fe3+ions, shared between octahedral and tetrahedral sites, while maghemite (-Fe2O3) can be considered as oxidized magnetite, due to Fe2+oxidation, being composedonly by Fe3+. Despite this, both have the cubic structure practically preserved, although in maghemite, the displacement of 11.1% of the iron creates vacancies that appear rather in the octahedral sites. The co-existing magnetite and maghemite resolution and identification are also complex due to the existence of a complete solid solution series between these two phases20,21. It has been shown that it is possible to distinguish iron oxidation states by EELS using a monochromatic (0.3eV) electron sourcein an electron microscope29. The microscope used in this study does not allow us to determine this; the energetic resolution reached is at best 0.9eV. Moreover, semi quantitative analysis (Fig.6B,D) showed that the concentration of iron is higher outside the cavities, which makes it possible to conclude that there was a migration of iron along the magnetosome crystal. Gallagher et al.18 showed that the formation of maghemite is controlled by the diffusion of iron cations. Shidu et al.21, confirmed this mechanism by following the evolution of the content in Fe2+during oxidation and the formation of a hollow structure resulting of the diffusion of Fe2+cations. As has been showed in the case of metallic nanostructures, the oxidation process leads to the formation of a hollow structure through a nanoscale Kirkendalleffect30,31. This phenomenon is explained by the differential of diffusion between the outward metal cations and the inward anions, such as oxygen. Their weaker effusivity is compensated by a flux of vacancies that condenses to form a hollow structure. In our case, a similar process is envisaged during the oxidation: diffusion of Fe2+outwards the magnetite with the inward diffusion of oxygen and vacancies that condense to form a hollow structure and formation of mixed oxides magnetite/maghemite on the surface of the nanocrystal of magnetite.

Considering the relevance of our results to paleomagnetism, the fact that magnetosomeretains its intact structure up to 300C under oxidizing conditions, confirmed the contribution of magnetotactic microorganisms to the magnetization of sediments as well as a record of ancient ecosystemsas proposed by Stolz et al.32. The [111] elongation direction of the crystal can be also determined by using the FFT from the high-resolution images (Fig.1G). Psfai et al.33 discussed that elongation of magnetosomes in magnetotactic bacteria is parallel to the [111] crystal axis for the equidimensional (cuboctahedral and octahedral magnetosomes) and elongated-prismatic shapes, while the elongation axes in anisotropic magnetosomes could be <100>, <110>, or <111>. The easy axis of magnetite magnetization is parallel to <111> axis. Thus, magnetite magnetosomes that present this characteristic can be considered the most evolved from the evolutionary point of view33. <111> is also the elongation axis of most magnetite mineralized abiotically; however, crystal morphology and dimensions of these particles are not similar to those biomineralized by magnetotactic bacteria. Elongation axis, shape and size of each type of magnetosome seem to be related to the evolution of magnetotactic bacteria and are considered as a signature of biogenic magnetite33. According to our results, exposure to temperatures of approximately 500C partially transforms the crystalline structure of magnetosomes. However, after this treatment, the obtained hollow structure partially retains the memory of the original magnetite structure as shown by its elongated morphology and the associated FFT (Fig.5D,E),which can be interpreted as resulting from magnetite or maghemite because their structures are very close. Indeed, this transformation is a topotactic transformation that retains the starting structure34.

It is important to note that, to definitively confirm the oxidation of magnetite in maghemite, the quantitative use of other more macroscopic techniques such as ex situ synchrotron X-ray diffraction associated with magnetometry techniques and Mossbauer spectroscopy is mandatory, but these analyses require a large amount of magnetosomes.

Therefore, our results showed that even if a magnetofossil has been subjected to extreme conditions, for example, entrance in Earths atmosphere, it might be possible to predict its biological origin, since crystallographic information is resistant to high temperatures, even if localized damaged caused by heat, as cavities observed in this study occurs. Thomas-Kepra et al.35 reported the presence of magnetite nanocrystals resembling magnetosomes in the Martian ALH84001 meteorite and suggested the existence of carbonate globules and rims in the meteorite, which might have protected magnetofossil from damage. Results presented here probably will help researchers in identifying magnetofossils damaged by high temperatures in relevant specimens, contributing to future analysis of extra-terrestrial or extreme environments fossil record.

From the biotechnological point of view, our results showed that magnetosomes can be subjected to high temperature and still maintain their structural and chemical characteristics, and, consequently, their magnetic properties. In nanomedicine, temperatures higher than 100C will probably not be applied, thus the use of magnetosomes as thermo-controlled drug-delivery systems, as proposed by Santos et al.36 with artificially synthesized superparamagnetic iron oxide nanoparticles, and magnetic hyperthermia probably would avoid the need of constant administration of the nano-formulation in the organism during treatment. The benefit of resistance to temperatures between 300 and 500C is directly related to the industrial application of magnetosomes to the recovery of molecules or metals and in nanobiocatalysis processes. Yoshino et al.37 developed a thermoresponsive magnetosome in which the elastin-like polypeptide was expressed in the surface of the magnetosome. At temperatures above 60C, the hydrophobicity of these nanoparticles increased, promoting their aggregation. According to our results, temperature up to 300C would be safe to maintain the magnetosome structure, and thus guarantee easy recovery and reuse of this biotechnological tool. Magnetosomes usage in biotechnological application is considered advantageous over artificially synthesized magnetite nanocrystals, because of their easy and effective functionalization, relatively cheap and ecologically-safe production, unique magnetic properties, narrow size and shape distribution and low aggregation between particles due to the presence ofthe bilipid layer. Thus, the results presented in this study showed the good thermal stability of magnetosomes and promising application in the development of stable nano-enzymatic complexes.Possibly, magnetosomes could be used in the improvement of nano-enzymatic complexes developed by the immobilization of structurally-stable hydrolases onto artificially synthesized nanoparticles that showed imprecise results regarding efficiency stability and reuse38.

In summary, the results presented here define a temperature range up to 300C as safe to maintain magnetosome structure preservation, which would ensure easy retrieval and reuse of this biotechnological tool in industrial applications that employ high temperatures. In addition, this work exhibits the employment of ground-breaking nanoanalytical in situ and 3D-TEM techniques for characterization studies of biogenic nanomaterials.

Cells of Magnetovibrio blakemorei strain MV-1 were grown in a 5L bioreactor (Minifors, Infors HT, Basel, Switzerland) as described previously39. After 192h of incubation, cells were collected by centrifugation (7,000 x g) and resuspended in 50mL HEPES buffer (10mM; pH 6.8). Cells were then disrupted by sonication (VCX 500, Sonics, Newtown, USA) at 20% amplitude and 20kHz frequency for 1h (60 cycles of 30s between intervals of 30s). Magnetosomes were magnetically concentrated for 12h at 4C with a neodymium-boron magnet attached to the bottom of the tube containing the magnetosomes. The supernatant was replaced by HEPES buffer (10mM) with NaCl (200mM), washed 4 times in a bench sonicator (Branson 2200) for 30min (each washing step) and concentrated again using the same magnet. Finally, supernatant was discarded and the magnetosomes resuspended in distilled, deionized H2O (1mL).

Magnetosome purification was verified by depositing magnetosome suspension (10L) directly on a formvar-coated copper grid (Electron Microscopy Sciences, USA), and observing this sample in a Morgagni transmission electron microscope (FEI Company, Hillsboro, OR, USA) with an acceleration voltage of 80kV.

For the thermal stability in situ evaluation, the extracted magnetosome suspension (1L) was deposited on a Si3N4 membrane of the E-chip used for the environmental gas analysis and air-dried for 1h. The in-situ experiments observations were carried out using a Protochips Atmosphere Gas Cell device. This later allows to heat the sample under controlled gas flow in the gas cell device. All the indicated temperatures are based on the company provided calibration. The microscope used for samples examination was a Jeol 2100F FEG equipped with a spherical aberration corrector, operating at 200kV in CTEM and in the BF-STEM or HAADF-STEM modes with a resolution of 0.11nm. Three types of experiments were carried out using the conventional TEM (CTEM), scanning TEM(STEM) and STEM tomography. Initially, argon gas (1atm pressure) was inserted into the in situ chip chamber and the temperature was raised to 150C. After 1h, the Ar was replaced by O2 (1atm pressure) and the samples were exposed to the following temperatures: 150, 200, 300 and 500C. During the experiment various CTEM images were systematically acquired under controlledirradiation conditions to evaluate the effect of the electron beam irradiation on the magnetosome structure. Finally, at 500C in the areas corresponding to the periodically irradiated region, high-resolution images were acquired. All images were obtained while the sample was at high temperature, excepting those acquired simultaneously to the energy-dispersive X-ray spectroscopy (EDS) analysis. For EDS measurement, we removed the silicon nitride window of the holders chamber to maximize the signal to noise ratio in the spectra by increasing the amount of X-rays emitted by the sample and acquired by the detector. A Silicon Drift Detector (SDD-EDS) was used to obtain X-ray (EDS) and a Gatan Imaging Filter (GIF) (Gatan Inc., Pleasanton, CA, USA) with 0.9eV energy resolution was used to obtain EELS spectra. Digital Micrograph software (Gatan Inc., Pleasanton, CA, USA) and JEMS software (http://www.jems-saas.ch/) were used to quantitatively analyse the images. The tomography was performed in HAADF-STEM mode by considering the angular range from 55 to +55 with a step of 1.5 between two successive images.

Jovane, L., Florindo, F., Bazylinski, D. A. & Lins, U. Prismatic magnetite magnetosomes from cultivated Magnetovibrio blakemorei strain MV-1: a magnetic fingerprint in marine sediments. Environ. Microbiol. Rep. 4, 664668 (2012).

Kopp, R. E. et al. Magnetofossil spike during the Paleocene-Eocene thermal maximum: Ferromagnetic resonance, rock magnetic, and electron microscopy evidence from Ancora, New Jersey, United States. Paleoceanography 22, PA4103 (2007).

Savian, J. F. et al. Environmental magnetic implications of magnetofossil occurrence during the Middle Eocene Climatic Optimum (MECO) in pelagic sediments from the equatorial Indian Ocean. Palaeogeogr Palaeoclimatol Palaeoecol. 441, 212222 (2016).

Sun, J. B. et al. Preparation and antitumor efficiency evaluation of doxorubicinloaded bacterial magnetosomes: Magnetic nanoparticles as drug carriers isolated from Magnetospirillum gryphiswaldense. Biotechnol. Bioeng. 101, 13131320 (2008).

Alphandry, E., Faure, S., Seksek, O., Guyot, F. & Chebbi, I. Chains of magnetosomes extracted from AMB-1 magnetotactic bacteria for application in alternative magnetic field cancer therapy. ACS nano 5, 62796296 (2011).

Honda, T., Tanaka, T. & Yoshino, T. Stoichiometrically controlled immobilization of multiple enzymes on magnetic nanoparticles by the magnetosome display system for efficient cellulose hydrolysis. Biomacromolecules 16, 38633868 (2015).

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Kumari, A. et al. Multiple thermostable enzyme hydrolases on magnetic nanoparticles: An immobilized enzyme-mediated approach to saccharification through simultaneous xylanase, cellulase and amylolytic glucanotransferase action. Int. J. Biol. Macromol. 120, 16501658 (2018).

Silva, K. T. et al. Optimization of magnetosome production and growth by the magnetotactic vibrio Magnetovibrio blakemorei strain MV-1 through a statistics-based experimental design. J. Appl. Environ. Microbiol. 79, 28232827 (2013).

This work was supported by CNPq, CAPES, FAPERJ, Instituto Nacional de Cincia e Tecnologia em Medicina Regenerativa/INCT-REGENERA, Rio de Janeiro, Brazil and the international associated laboratory Advanced Electron Microscopy of Biomaterials (AEMB) between the CNRS and University of Strasbourg (France) and UFRJ (Brazil). D.A.B. is supported by US National Science Foundation (NSF) grant EAR-1423939.

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the articles Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the articles Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Cypriano, J., Bahri, M., Dembel, K. et al. Insight on thermal stability of magnetite magnetosomes: implications for the fossil record and biotechnology. Sci Rep 10, 6706 (2020). https://doi.org/10.1038/s41598-020-63531-5

odr as an effective method to ensure access to justice: the worrying, but promising brazilian case

Alternative Dispute Resolution (ADR) is the use of mechanisms to resolve disputes such as conciliation, mediation, arbitration and even negotiation without the involvement of the state and its judiciary. While ADR methods have returned to the spotlight over the last 20 years, the truth is that they precede the emergence of our society)[3].

In fact, although there is no precise record indicating the exact moment these methods arose in the history of humanity, there are indications that their use precedes the emergence of the democratic state of law and its institutions. The reason for this is simple: since, among the ancient peoples, there was no organized state with a formal judicial structure, alternative forms of settlement were used to resolve conflicts between people.

Throughout history, mercantilist policies have rendered ADR methods either obsolete or complementary to the judicial complex, since the intervening state needed to maintain the jurisdictional monopoly. Given that the sovereign state as we know it today has not always existed, it is possible that ADR methods are in fact the traditional methods of dispute resolution.

The arrival of the internet age has posed many new challenges as a larger part of the economy has started to operate online and transnationally with a new framework emerging. The internet is not a technology per se, but a network that unites several pillars of innovation. The first of these pillars was built by engineers and scientists from the Advanced Research Projects Agency (ARPA), which, in the late 1970s, created the first peer-to-peer (p2p) connection between computers.

After the spread of the global computer network and the rise of online business activities and operations, it became necessary that disputes between contracting parties be resolved online cheaply, quickly and efficiently thereby culminating in ODRs development.

The precursors of ODR were Professors Ethan Katsh and Janet Rifkin, who, in 1997, founded the National Center for Technology and Dispute Resolution (NCDR), linked to the University of Massachusetts, with the goal of fostering information technology and conflict management, and who wrote the first book on the subject in 2001[4]. After this, several renowned institutions began to explore ODR, such as the United States Department of Commerce, the World Intellectual Property Organization (WIPO), and the Hague Conference on Private International Law[5].

ODR (Online Dispute Resolution) has been gaining wider acceptance in conflict resolution, especially in the e-commerce context. However, while old disputes are vanishing from society (e.g., which neighbor owns the fruit from a tree on the boundary of their properties) new disputes are exponentially being created by the interconnection of the world and the inclusion of more individuals on the world wide web. One cannot deny that innovation is boosting conflicts across the globe.

Bearinginmindthis frenzy of disputes, the International Chamber of Commerce (ICC) organized in June 2017 a conference titled Equal access to information and justice, online dispute resolution in which stakeholders from more than 30 countries discussed the progress of ODR[6]. Due to the new requirements of operations and contracts established on the internet, understanding ODR and its techniques becomes, above all, the new dispute resolution lawyers duty.

This trend has four pillars, which can be summarized as (i) the virtualization of the courts, (ii) the use of decision-making algorithms, (iii) the use of big data for dispute prevention[7] and (iv) free access to legal information[8].

To clarify how this new method works, SquareTrade is a successful and practical example used by the giant eBay[9], an electronic commerce company that enables an enrolled user to advertise, to sell and to acquire goods.

The Ebay Resolution Center resolves an incredible amout of over 60 million disputes per year, making it one of the biggest ODR systems in the world. How does it work? As an Ebay seller you must refer costumers to its ODRs platform. The buyer needs to file a complaint by following these two steps: (i) creating a SquareTrader User ID and password and (ii) entering complaint details. After that, SquareTrade will send a notification email to the other party so it can respond the customer.

The complaint and the response will appear in a secure area on the SquareTrade websites and only the parties and the mediator (if they choose to involve one) will be granted access. The mediator costs about USD 15 and the whole process generally takes 10 days.

Alibaba also has an ODR tool for settling disputes between sellers and buyers who use that marketplace. The buyer can open a dispute after making payment and before confirming delivery of its order in two cases: (i) the goods are not received before the shipping deadline or (ii) the goods are not received with fulfillment of the conditions predicted. If the parties cannot resolve a complaint within 10 days, a panel of Alibaba's ODR team settles it by imposing penalties on the defaulting party[10].

Both Ebay and Alibaba solve their conflicts in an impersonal, objective and predictable way at a rate of approximately 90% of settlements. An important point in this regard is that the more conflicts they resolve, the more their algorithms collect data that serves to provide more precise responses, improving the settlements and arbitrations, when necessary. The low cost is also an important online dispute resolution incentive since the costs in the Brazilian justice system would be minimally lower or the same.

In the public sector, ODR has also been growing. Fifteen years ago, the Money Claim Online program was set up by the Ministry of Justice of England and Wales in order to allow users to open protocols equivalent to collection actions in the amount of up to GBP 100,000.

The Money Claim Program is an online charge model that starts with the elaboration of an online form by the lender. After that, the debtor receives a subpoena, which, if not responded to, leads to an enforceable title. Virtual court statistics are extremely positive: they are able to resolve more than 60,000 cases a year.[11] In the Canadian province of British Columbia, the first online tribunal, the Civil Resolution Tribunal (CRT), has been operating since 2016, accepting claims of up to CAD 5,000, aside from condominium disputes, which have no pre-specified amount.

The procedure requires different steps. The first is called solution explorer, when the algorithm analyses the complaint and offer information and solutions for the problem. After that is the dispute resolution tool in which an online negotiation tool comes into action. By this point, the users already have much more legal information and the capability of problem framing than when litigating in the judicial system.

If the parties cannot reach an agreement, there is a third step called facilitation, where human intervention is necessary to attempt to reach an agreement. And, if the dispute still unresolved, the case will be decided by a third impartial party.

It is important to note that, although ODR is expanding, its methods are still restricted to simpler controversies that can be adapted to pre-defined parameters. Its use so far is not viable for complex cases with large values at stake, which require extensive evidence production. On the contrary, simple litigation cases involving consumer law, for example, which can overwhelm the judiciary and could easily be resolved, are good candidates for resolution by ODR. Conventional litigation for these cases can be quite costly, time consuming and inefficient, proving ODR to be the most efficient solution.

Scholars Brian Garth and Mauro Cappelletti identified three key obstacles to access to justice: cost, organizational problems and a lack of adequate procedures[12]. Unlike most modern jurisdictions, the costs incurred by plaintiffs are not an obstacle in Brazil, but organizational problems and adequate procedures are.

To property understand that, it is important to distinguish "access to justice" from "access to courts". "Access to justice" involves not only access to the judiciary branch ("access to courts"), but also broad public access to legal information and the protection of individual rights, which lies in the utilization of other means of social peace and conflict resolution[13]. Within the inevitable problems involving a court case anywhere in the world, i.e. bureaucratic delays and asymmetric information, the reach of the access to justice goal must take place outside of the courts and through a realistic and efficient method of dispute resolution.

The promulgation of the Brazilian Constitution established "access to justice" as a fundamental right that should be available to by every stakeholder of democracy. In light of that, well structured Public Defender Offices have been created to ensure that all citizens regardless their financial situation can be represented in a lawsuit for free, provided that they can prove they cannot afford to litigate before a court without compromising their livelihood.

In addition, the Small Claims Court Act (Brazilian Federal Law No. 9,099 from 1995) established a new type of court for lawsuits where the amounts in dispute are lower than 40 times the minimum wage in Brazil ( approximately USD 15,000.00). Parties who wish to see their disputes settled before a Small Claim Court do not have to pay court fees, and, if the amount claimed is lower than 20 times the minimum wage, they do not need a lead lawyer to file the lawsuit.

These apparently optimistic scenarios worsened the crisis of the Brazilian Judiciary Branch by absurdly increasing the number of ongoing proceedings. Legitimate claims often have to wait for years to go to trial, while the courts are buried with sham litigation and groundless pleadings. The Justice Luis Felipe Salomo from the Brazilian Superior Court of Justice once affirmed during an interview that companies took this unfair advantage and turned the courts into their call centers[14].

In spite of serious efforts, ADR did not change this situation in Brazil either. Arbitration has been present in the Brazilian legal system for almost 200 years in various non-specific legal compilations (e.g article 1603 of the 1824 Brazilian Constitution). However, it was only in 1996 that Brazilian Law No. 9,307/96, also known as Arbitration Act, institutionalized it. Nevertheless, the aforementioned Act was only fully implemented after a controversial battle before the Supreme Court, in which it was argued that section XXXV of article 4 of the 1988 Brazilian Constitution, which states that "the law shall not exclude from the assessment of the Judicial Branch any injury or threat, was in conflict with arbitration. The constitutionality of arbitration was granted during the trial of the Contested Foreign Award from the Kingdom of Spain n 5206-8/247.5 Despite this, arbitration in Brazil is still reserved for complex litigation involving large sums of money due to its cost and the prohibition of the procedure for consumer relation disputes.

Mediation also is not a successful patth, at least yet, for the reduction of litigation in Brazil. Despite the promulgation of the Brazilian Mediation Act of 2015, there are few qualified mediators, and theyre involved mainly in big corporate disputes instead of settling small conflicts. In addition, many Brazilian citizens believe wrongfully that mediation is attached to court proceedings, something like a pre-trial hearing.

In addition, the internet age is exponentially increasing the connectivity of society and the number of transactions conducted. If someone once took two hours to buy a book at a bookstore, today he or she can do it online in less than five minutes at a much lower cost. It is also likely that this person would buy many more books. But, Colin Rule stated, where there is commerce, there is conflict[15].

When we look at the implementation of ODR services, there are two factors that must be taken into account: (1) Information and Communications Technologies (ICTs) and (2) the local digital economy. Both give an indication as to how quickly the ODR infrastructure is developing, especially when considering its use to resolve disputes involving online and offline commerce. In Latin America, for example, the number of new internet users grows daily. By the end of 2010, there were approximately 181 million users, suggesting that the digital economy is booming.[16]

According to the Justice in Numbers 2016 report published by the National Justice Council (CNJ), court litigation represents a cost of 1,3% of the Brazilian GDP[17]. Also, a study published in 2016 by Valor Econmico (a leading business newspaper) anual, entitled The Costs of Court Litigation to Organizations[18] states that the Brazilian Justice System has about 100 million cases. If we consider that in 2014 companies spent close to BRL 124,81 billion (approximately USD 35 billion) in litigation, it is not too difficult to understand why the need for changes and improvements has become not only urgent, but also acceptable by nearly all the parties involved to ensure economic growth.

Overall and taking into consideration only the labor and contractual disputes, consumer cases rank in third place amongst those faced by Brazilian companies and, in Rio de Janeiro alone, the second largest Brazilian State, over five hundred thousand new cases are filed every year.

Notwithstanding that, the Brazilian Judiciary Branch is stagnant in the last century. Although the Law No. 11,419/06 (Electronic Procedure Act) was enacted more than ten years ago, little has changed in terms of procedural speed since the electronic procedure merely replicated the steps of an offline lawsuit. Without any cognitive computing apparatus, document automation and data science to facilitate processing and decision, judges are being inundated with new lawsuits in a number that has grown exponentially since the enactment of this law[19].

Fortunately, in August 2017, during the Conference on Civil Procedural Law organized by the Brazilian Federal Justice Council (CJF), Statement No. 25 was approved, which provides that conciliation or mediation hearings may be held by videoconference, audio, exchange of messages, online conversation, writing, electronic means telephone or other mechanisms that serve the purpose of self-composition[20]. This measure allows more bold approaches by judges to technology be carried out during their court proceedings.

In the same sense, in order to try to decrease such a high demand of pending and new cases, the CNJ (National Justice Council) enacted the Resolution No. 125/2010, which regulates the Judicial Policy for the Treatment of Conflicts, which was recently updated. On its Amendment number 2, as well as several other important adjustments, the Digital Mediation System was introduced for allowing pre-procedural resolution of conflicts and for consensual action in ongoing legal proceedings in the interest of each court.

However, there is a strong resistance to ODR methods so the legal market demand for negotiating platform agreements is only 2%[21] according to recent research carried out by the Brazilian Association of Lawtechs & Legaltechs (AB2L). This happens not only because of a lack of knowledge about the method itself and the benefits inherent in this type of dispute settlement[22], but also because of the traditional and old school mindset of lawyers. As stated in the beginning of this article, not much has changed in the dispute resolution framework in the last millennia; if you stop for a minute and think, you will notice that we still attend a hearing in-person at a pre-set location at an appointed time and submit hard, copy documents before a panel of elderly people.

There is an ocean of opportunities for improvement of dispute resolution through technology that we need to embrace. Nevertheless, if you cannot believe that digitalization of justice is a relentless reality for the near future, do not feel guilty. Due to the cognitive bias of human reasoning known as the availability heuristic, we tend to doubt something until we have experienced it since our switch to reality is what we have available at the time.

Over the last several years, each technology improvement in the Brazilian Judicial Justice System was received with riots and outcries generated by the lawyers. It happened when the Electronic Procedure Act was enacted and it happened recently with the attempt of the implementation of an Online Court in the State Court of Rio de Janeiro[23]. People tend to maintain old-fashioned yet updated practices even though there are more efficient ways of doing it (status quo bias)[24]. However, it did not happen only in Brazil. Professor Richard Susskind once said that he was almost disbarred from the Law Society of England and Wales for defending the during the 1990s that e-mails would be the main form of communication between clients and attorneys. His peers alleged that he was disrespecting the legal community by waiving the attorney-client privilege[25]. The greatest challenge is not technological, however, it relies on the lawyers mindset.

If we increasingly use the internet and all its functions, which, by the way, are becoming closer and closer at an astonishing speed in a short time, ODR will occupy a relevant space in dispute settlement. In Brazil, arbitration took approximately fifteen years to go mainstream; mediation is still crawling. ODR cannot afford not to evolve and not to be popularized at the same pace as innovation, otherwise the Brazilian Justice System will simply stop working, while its citizens will be isolated from one of the most fundamental rights of modern societies: access to justice.

Technology has come to the legal field to stay, and if the court proceedings are the civilized form that mankind has found to make war and ADR is a way to rationalize it, digitalization of dispute resolution is in its advanced form. ODR methods will undoubtedly serve to improve access to justice since these methods are capable of reducing the judicialization of ordinary conflicts of a simpler nature. From a social perspective, it is necessary to question whether investing a large part of our limited public resources in the Judiciary is, in fact, appropriate when there are faster and less expensive alternatives available.

[2] Daniel Becker is an associate in the Rio de Janeiro office of Tauil & Chequer Advogados in Association with Mayer Brown LPPs Litigation and Arbitration practices. He holds a degree in Law from the Federal University of Rio de Janeiro (UFRJ) and is currently pursuing his LL.M in public law at FGV School of Law. He participated in the XIX and XX Willem C. Vis International Commercial Arbitration Moot as a team member representing his university. Daniel Becker is the Director of New Technologies in the Brazilian Center of Mediation and Arbitration (CBMA), a member of the Silicon Valley Arbitration and Mediation Center (SVAMC), and a former Vice-President of the Brazilian Association of Arbitration Students (ABEArb) and the Young Arbitrators Committee of CBMA (CJA/CBMA).

[3] Daniel Becker and Pedro Lameiro, Online Dispute Resolution (ODR) e a ruptura no ecossistema da resoluo de disputas, acessed 28 December 2017.

[5] Julio Csar Betancourt and Elina Zlatanska. Online Dispute Resolution (ODR): What is it, and is it the Way Forward? (2013) International Journal of Arbitration, Mediation and Dispute Management, Issue 3/2013 acessed 01 May 2017.

[6] Mirze Philippe. Equal Access to Information & Justice: The Huge Potential of Online Dispute Resolution Greatly Underexplored (I). Kluwer Arbitration Blog. acessed 12 September 2017.

[14] Rodrigo Haidar.Empresas transferiram seu call center para o Judicirio Consultor Jurdico acessed 29 October 2017.

[15] Thomas Claburn, Modria's Fairness Engine: Justice On Demand. Information week. acessed 29 de October 2017.

[17] Fbio Vasconcellos.Na relao com o PIB, Judicirio brasileiro custa quatro vezes o registrado na Alemanha O Globo acessed 29 de October 2017.

[21] Startupi. AB2L apresenta primeira pesquisa nacional sobre o cenrio de lawtechs e legaltechs StartUpi acessed 28 December 2017.

Daniel Becker is an associate in the Rio de Janeiro office of Tauil & Chequer Advogados in association with Mayer Brown. He is a member of the Litigation & Dispute Resolution and International Arbitration practices. His work involves representing clients in arbitration and judicial proceedings in Brazil and abroad, in complex matters related to various industry sectors. Daniel has a considerable experience with regulations and dispute resolution in the technology industry. He has represented several companies in multi-litigation cases and class actions arising from critical events. He has also advised a major Brazilian marketplace company on the compliance with the UE General Data Protection Regulation (GDPR). Daniel Becker currently lectures about Technology Law on several Brazilian universities in Rio de Janeiro and So Paulo. Daniel is currently the Director of IT Law at the Brazilian Center of Arbitration and Mediation (CBMA). He is pursuing a LLM on Public Law before FGV Direito Rio and he is graduated from the Federal University of Rio de Janeiro (UFRJ).

Andrea Maia is a proven performer, capable negotiator, and strategic thinker with a solid experience and academic background in law, business and conflict resolution. Sixteen years of experience in Corporate Law, covering a variety of industries such as Aviation and Banking, either as a Corporate Lawyer in large organizations such as Embraer and Banco Opportunity; or through her own practice, with a variety of large and small clients, including Jornal do Brasil. Currently works in mediation, negotiation and Alternative Dispute Resolution as a founding partner at FindResolution.

achieving global malaria eradication in changing landscapes | malaria journal | full text

Land use and land cover changes, such as deforestation, agricultural expansion and urbanization, are one of the largest anthropogenic environmental changes globally. Recent initiatives to evaluate the feasibility of malaria eradication have highlighted impacts of landscape changes on malaria transmission and the potential of these changes to undermine malaria control and elimination efforts. Multisectoral approaches are needed to detect and minimize negative impacts of land use and land cover changes on malaria transmission while supporting development aiding malaria control, elimination and ultimately eradication. Pathways through which land use and land cover changes disrupt social and ecological systems to increase or decrease malaria risks are outlined, identifying priorities and opportunities for a global malaria eradication campaign. The impacts of land use and land cover changes on malaria transmission are complex and highly context-specific, with effects changing over time and space. Landscape changes are only one element of a complex development process with wider economic and social dimensions affecting human health and wellbeing. While deforestation and other landscape changes threaten to undermine malaria control efforts and have driven the emergence of zoonotic malaria, most of the malaria elimination successes have been underpinned by agricultural development and land management. Malaria eradication is not feasible without addressing these changing risks while, conversely, consideration of malaria impacts in land management decisions has the potential to significantly accelerate progress towards eradication. Multisectoral cooperation and approaches to linking malaria control and environmental science, such as conducting locally relevant ecological monitoring, integrating landscape data into malaria surveillance systems and designing environmental management strategies to reduce malaria burdens, are essential to achieve malaria eradication.

Malaria continues to be a major public health burden globally, with over 200 million cases in 2018. Despite effective treatment and control measures, over 400,000 deaths are caused by malaria annually, primarily in sub-Saharan Africa [1]. Malaria eradication, the permanent reduction of malaria infections globally to zero, has been a long-standing goal of the public health community, with a previous failed malaria eradication attempt from 19551969 [2]. Following significant reductions in malaria morbidity and mortality between 2000 and 2015, the World Health Assembly endorsed aims to reduce malaria burdens a further 90% by 2030 and has again begun exploring the possibility of malaria eradication [3]. Within the past year, two separate initiatives, the World Health Organization (WHO) Strategic Advisory Group for Malaria Eradication (SAGme) and the Lancet Commission on Malaria Eradication analysed future scenarios, concluding that malaria eradication is feasible and outlining key priorities [4, 5]. Both reports examine the impacts of global environmental change and conclude long-term climate patterns and urbanization are likely to be favourable for malaria eradication. Within these assessments, land use and land cover changes (LULCC) are only recognized as external factors influencing malaria transmission and not as a priority for eradication campaigns due to the difficulty predicting impacts.

LULCC, such as deforestation, agricultural expansion and infrastructure development, have huge potential to impact malaria control efforts through disruptions of both ecological and social systems [6]. Natural geographic heterogeneity in malaria is largely driven by biological differences in Anopheles species adapted to different landscapes while human vulnerability, economic status and access to healthcare are intricately linked with local environmental factors. The efficacy of malaria interventions and vector control measures are largely dependent on these factors and a successful malaria eradication campaign needs to develop landscape-specific strategies. Within countries moving towards elimination, many remaining foci of malaria transmission are driven by landscape factors, such as the high malaria incidence associated with deforestation in Southeast Asia and South America [7]. Conversely, many major malaria elimination successes were underpinned by LULCC, including, famously, the extensive hydrological and agricultural modifications conducted by Italian malaria control programmes following World War II [8]. Because LULCC are dynamic processes, impacts on transmission change over time following initial environmental changes and subsequent development. Anthropogenic changes generally reduce biodiversity, favouring species adapted to human populations. As land is transformed at unprecedented rates, there is a danger that future development will embed malaria into these landscapes, creating ideal man-made habitats for Anopheles vectors. Alternatively, the expected extent of future development offers unparalleled opportunities to build out malaria, reducing background transmission sufficiently to enable malaria eradication.

In this article, based on a report commissioned by the SAGme, a framework is outlined for incorporating LULCC into malaria eradication strategies. While previous successful disease eradication programmes for smallpox and rinderpest relied heavily on vaccination, there remains no highly effective licensed vaccine for malaria and increasing levels of insecticide resistance threaten to undermine existing vector control methods [9]. Emergence of zoonotic malaria in Southeast and South America presents new challenges for eradication and requires explicit consideration of LULCC on wildlife habitats. Within this context, it is clear a successful malaria eradication strategy will need to both mitigate the negative impacts of LULCC and leverage LULCC beneficial to malaria control. Effective strategies are inherently interdisciplinary and cannot be implemented solely within health sectors, requiring engagement of agricultural scientists, engineers, geographers and other disciplines to monitor and mitigate impacts of LULCC on malaria transmission [10]. Although interactions between human and natural systems driving malaria transmission are undoubtedly complex, this should not preclude explicit consideration of LULCC into eradication strategies. This article outlines the extent and drivers of LULCC, review the evidence on direct and indirect impacts on malaria transmission and identify priorities for malaria control and eradication, using landscape data to inform malaria surveillance and control while in turn incorporating malaria risks into land management strategies.

Land cover refers to the physical and biological cover of terrestrial surfaces, such as water, soil, vegetation and infrastructure, while land use refers to the human management and activities which modify land surface processes [11]. Although people have transformed landscapes since prehistoric times, the extensive changes in the past 300years following the Industrial Revolution have been unprecedented, leading to this era being termed the Anthropocene [12]. While agricultural land occupied less than 2% of global ice-free land prior to 1000 AD, this percentage increased to over 4% in 1700 AD to 35% in 2000 AD [13]. Today, over 75% of Earths ice-free land has been altered by human residence and land use [14].

Deforestation remains one of the main global LULCC (Fig.1). Changes to forest cover are particularly pronounced in tropical areas, where over 80% of new agricultural land was cleared from tropical rainforests between 1980 and 2000 and an estimated 2100 km2 of forests were lost per year between 2000 and 2012 [15, 16]. Much of this deforestation is driven by agricultural expansion driven by rising demands due to population growth and increased consumption levels [17]. Between 1970 and 2010, there has been a 1.4-fold increase in the number of livestock and an 18.4% increase in daily per capita food availability globally [18]. However, increased productivity and industrialization has meant this increase in the amount of food produced is not always accompanied by corresponding increases in land area but rather new management techniques, such as irrigation and fertilizers [19]. For example, there was a 73% increase in the area of irrigated land between 1970 and 2010 [20]. Global biofuel production is also increasing rapidly, growing 19.4% per year globally between 2004 and 2011, with an expansion of 33.2 million hectares for oilseeds globally [21].

The causes for LULCC are multifactorial, with underlying political, institutional and economic factors driving agricultural expansion, resource extraction and infrastructure development [22]. For example, while extensive deforestation occurred in Indonesia between 2000 and 2012, commitments to global climate change agreements led to substantial decreases in forest loss in 2017 [23,24,25]. Conversely, policies may have unintended implications. Peace agreements between the Colombian government and armed groups led to land colonization in previously inaccessible areas of the Andean-Amazonian foothills of Colombia; deforestation has been further amplified by governmental programs building roads and fostering extractive and ranching industries [26]. United States drug policies have led to narco-deforestation, extensive forest loss in Central America fuelled by the development of landing strips, need to launder money and influxes of cash from the global narcotics trade [27]. These complex economic and social forces driving LULCC may have unintended consequences for malaria transmission, disrupting both ecological and human systems (Table 1).

Impacts on malaria transmission are complex and highly context-specific, with environmental and demographic changes within a specific setting either increasing or decreasing risks. Natural geographical variation is largely driven by biological differences between local Anopheles species and the landscapes to which they are adapted. LULCC changes affect these disease systems in different ways in different regions. For example, when a landscape becomes urbanized, the original natural streams and ponds are typically either drained, enclosed in concrete, or polluted with decaying organic matter. These transformations make the water unsuitable as a breeding site for all-but-one Anopheles malaria vector species (though other mosquitoes such as Culex quinquefasciatus can thrive). For this reason, there is often little or no transmission in the thoroughly urbanized centres of large African cities, despite intense transmission in the surrounding countryside. In India, by contrast, there is Anopheles stephensi. the worlds only important Anopheles species that is well-adapted to urban conditions, through its ability to breed in man-made containers, including domestic water storage containers. Because of these differences in vector species, urbanization has different impacts on malaria geographically.

Anthropogenic LULCC is one element of a complex development process with economic, agricultural and social dimensions. As these components all affect malaria and occur simultaneously, it is difficult to distinguish between effects of landscape, housing, health coverage and other factors. In north-western Europe, malaria gradually disappeared between 1550 and 1950, not due to public health interventions, but from cumulative shifts in land use, including drainage of marshes, shifts in animal husbandry, and improvements in housing. Similarly, the introduction of house-spraying and improved drugs in the mid-twentieth century enabled elimination to be achieved in Southern Europe, the USA and several Caribbean islands. However, environmental, economic and social factors were equally important, reducing background transmission to the point where elimination was within reach and making malaria absence a stable state after the withdrawal of anti-malaria spraying despite the re-introduction of infection by imported cases. This section outlines how LULCC impacts vector, human and wildlife systems, highlighting the linkages between these.

LULCC directly affects anopheline mosquito populations, altering the abundance, species composition and life history of malaria vectors. Ecological changes in soil, sunlight cover, vegetation type, development of water pockets and water temperature, affect breeding conditions for Anopheles malaria vectors with effects varying by Anopheles species. For example, while deforestation reduces shaded water bodies, the preferred breeding habitats of some Anopheles species, other Anopheles species thrive in water bodies with increased sunlight, with increased larval survivorship, adult productivity, intrinsic growth rates and shortened gonotrophic cycles significantly increasing vectoral capacity [28]. Other environmental and microclimate changes due to LULCC may favour survival of different Anopheles species enabling sustained seasonal malaria transmission or impacting the availability of hosts and blood meals.

Associations between forest disturbance and vector ecology are widely described in Southeast Asia and South America. Many highly efficient forest vector species occur within these regions, breeding in forest fringe and deforested areas. For example, within Malaysian Borneo, Anopheles balabacensis biting rates were greater in modified forest than in primary forest, with breeding sites found in wheel tracks in logged areas [29]. Similarly, deforestation within the Amazon also resulted in increased larval breeding sites and corresponding increases in malaria incidence [30]. In the Peruvian Amazon, extensive deforestation between 1983 and 1995 undermined previous achievements of malaria eradication programmes and corresponded with a fourfold increase in malaria cases nationally between 1992 to 1997 and a 50-fold increase within the rapidly deforested Loreto Department [31]. This malaria emergence paralleled increases in Anopheles darlingi, which was not found in the area in 1991 and favours ecologically altered habitats, leading to increased vector density in areas undergoing rapid land use change in close proximity to human settlements [31].

However, in some sites, forest disturbance may reduce malaria risks. For example, in African sites where the deep forest species Anopheles nili is the main vector, deforestation leads to modest reductions in malaria transmission [7]. Alternatively, in other African sites, deforestation can create habitats for non-forest efficient vectors. In Nigeria, forest loss was demonstrated to have a large impact on malaria risks, with each standard deviation of forest loss corresponding to an almost 5% increase in malaria in children under 5 [32]. A study in the Democratic Republic of Congo similarly found deforestation and agricultural expansion led to an increase in malaria prevalence in children; these LULCC were associated with increases of indoor biting rates of the malaria vector Anopheles gambiae sensu lato [33].

Forest disturbance can also impact species composition and may initially deplete deep forest vectors but subsequently lead to invasion by other efficient vectors [7]. Counter-intuitively, the abundance of both colonist (disturbance-tolerant) and climax (disturbance-intolerant) anopheline mosquitoes species increased in disturbed forests in Panama [34]. Anopheles albimanus, a colonist species, co-existed at the landscape scale with two climax species, Anopheles oswaldoi and Anopheles triannulatus. The likelihood of colonist-vector species occurrence was most prominent at highly disturbed forest sites and decreased markedly in relatively undisturbed forest [34]. Similarly, a study in highly fragmented forested areas of Cambodia suggested decreases in primary malaria vectors but increases in secondary vectors, with the outdoor and early biting behaviours of these secondary vector species sufficient to maintain malaria transmission [35]. These impacts on species composition influence contact rates with hosts and pathogen transmission, with colonist species often more likely to transmit pathogens than climax species.

Agriculture has also been associated with changes in Anopheles densities due to factors such as planted crops, irrigation, applications of pesticides or changes in host availability. Rubber plantations, containing planted trees with high humidity and lower temperatures, can provide ideal environments for malaria vectors. Since the first accounts in Malaysia, regular malaria outbreaks have been reported across Southeast Asian rubber plantations [36]. As 90% of the global demand in rubber is met by the expansion of rubber plantations in Southeast Asia, with an expanding migrant workforce, malaria control in this region might be jeopardized by the rubber boom [36]. Introduction of new crop species or farming practices can also alter vector species composition. In Thailand in the 1970s, development of cassava and sugarcane plantations led to increases in malaria risks. While these agricultural changes decreased the density of the shade-loving species Anopheles dirus, the modified landscape provided ideal breeding conditions for the sun-loving Anopheles minimus and resulted in an increase in malaria transmission among resettled cultivators [28]. Other agricultural methods such as slash-and-burn techniques similarly lead to deep shade elimination, changes in the acidity and chemical composition of the soil, creation of new breeding sites in the forest fringes and higher host exposure [7]. However, while much of the literature focuses on agricultural practices driving malaria transmission, agricultural practices also can reduce transmission; for example, agroforestry is increasingly proposed as a malaria intervention in Africa where planting trees can both increase biodiversity and decrease breeding sites for sun-loving Anopheles vectors [37].

Irrigated rice cultivation can also create permanent habitats for mosquito larvae [38]. For example, prolongation of the breeding season of Anopheles aconitus caused by rice cultivation and its linked irrigation systems in Indonesia resulted in an increase of malaria incidence [28]. In sub-Saharan Africa, initiatives to systematically increase irrigated rice cultivation have resulted in a rise in prevalence of the malaria vector, Anopheles arabiensis. Agronomic practices, such as fertilizer and insecticide use, can increase available nutrients and create predator-free habitats, increasing larval density; conversely, use of pesticides against agricultural pests may also decrease mosquito populations. Additionally, gravid An. arabiensis are attracted to the odour of rice, acting as a cue for oviposition site selection [38]. However, the impacts of increased vector densities in agricultural settings on malaria transmission is unclear. Described as paddys paradox, in many cases, increased abundance may correlate with changes in biting patterns or life history or be counteracted by the socioeconomic and public health improvements associated with agriculture [39].

Wider developments of irrigation and water projects can also drive changes in vector ecology through mechanisms such as increased breeding sites, changes in water pH, turbidity and chemical composition [40]. Globally, since 1984, net increases in surface water was detected on all continents except Oceania, largely driven by reservoir creation. However, within these global trends, there are substantial fine-scale variations in changes in surface water levels and highly concentrated patterns of loss (Fig.2) [41]. Within sub-Saharan Africa, large dams have major malaria impacts in areas of unstable transmission, either by intensifying transmission or through shifting from seasonal to perennial patterns [40, 42]. Existing large dams were predicted to increase the risk of malaria for around 15 million people, adding more than 1 million cases annually to the malaria burden in the region, with an additional 50,000 cases per year resulting from planned dams.

These ecological changes are intricately linked with the distribution, movement and quality of life of human populations. LULCC can result in influxes of immunologically nave populations to undertake land conversion activities. This has been well described in the Brazilian Amazon, where policies encouraging development of the Amazon in the 1970s were linked to the explosive increase in malaria cases, from a total of 8,000 cases prior to the explicit government policy to up to 615,000 in the year 2000, with 99% of all malaria cases after 1990 reported in the Brazilian Amazon [43]. Termed frontier malaria, early stages of forest clearance are linked with changes in human exposure risks, weakened health systems and creation of vector breeding sites [44]. Risks of malaria are often highest during the initial stages of land clearing and settlement, decreasing with urbanization, agricultural expansion and increased socioeconomic status [45]. These frontier communities are often characterized by weak social institutions, limited health care and absence of malaria control measures [46].

Beyond mosquito ranges, malaria can be imported by human movements. Within the Brazilian Amazon, proximity and mobility between frontier settlements and activities explain malaria diffusion regionally [43]. Similarly, in the village of Cacao, French Guiana, a recently built road connecting the village with Brazil may have facilitated the movement of carriers from endemic areas [47]. On a national scale, analysis of mobile phone data across Kenya highlighted the role of human mobility in malaria transmission; these movement patterns are largely driven by trade and connectivity of different land use types [48].

LULCC is also accompanied by changes in specific risk behaviours and occupations as individuals undertake land conversion and agricultural activities. For example, disturbance of forest to increase farming surface has attracted seasonal workers into vector habitats in French Guiana. Risk behaviours among this migrant worker population such as outside kitchens, agricultural work during peak biting times and the absence of repellents or mosquito net use explained the spatial heterogeneity of malaria occurrence in this site [47]. Similar risk behaviours are seen among small scale gold miners in Brazil, with high population mobility facilitating parasite diffusion [43]. Within Southeast Asia, migrant workers and forest and plantation activities have similarly been identified as risk factors for malaria exposure (Fig.3) [35, 49].

Conversely, primarily driven by economic factors, LULCC can have correspondingly positive influences on human health. In many places, initial environmental changes are followed by increases in socioeconomic status and improvements in infrastructure and public health services. For example, expansion of irrigation systems in an arid region of India was associated with dramatic increases in malaria risks; however, over time, the economic prosperity from these developments and increased health service availability led to decreased malaria incidence [50]. Modelled impacts of deforestation in frontier regions including socioeconomic factors similarly predict initial increases in malaria transmission followed by decreases due to improved socioeconomic status [45]. Economic development can improve housing quality and infrastructure, factors associated with decreasing risks of malaria [51, 52]. While differing time scales may make untangling environmental and societal impacts on malaria transmission challenging, fully understanding risks of landscape changes requires assessing how these coupled human-environmental systems interact.

LULCC impacts on vector and human populations may be further amplified by wildlife malaria reservoirs. Although four main human malarias (Plasmodium falciparum, Plasmodium malariae, Plasmodium ovale and Plasmodium vivax) are widely recognized, zoonotic malaria species such as Plasmodium knowlesi and Plasmodium simium are emerging public health threats [53]. Genetic studies suggest that human malarias such as P. falciparum originated from great ape species and these human malarias continue to circulate in great ape and gorilla populations in West and Central Africa [54,55,56]. These close evolutionary relationships, coupled with increased spatial overlap between human and non-human primate populations, present future challenges to malaria eradication.

Dramatic increases in human Plasmodium knowlesi cases threaten to undermine progress towards malaria elimination in Southeast Asia. Plasmodium knowlesi is a malaria species maintained by long and pig-tailed macaques (Macaca fascicularis and Macaca nemestrina) and transmitted by the Anopheles leucosphyrus group of mosquitoes [57, 58]. Since the identification of a cluster of human P. knowlesi infections in Malaysian Borneo in 2004, sporadic cases have been reported across Southeast Asia and P. knowlesi is now the main cause of human malaria in Malaysia [59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75]. Recent molecular studies have additionally identified human infections with Plasmodium cynomolgi, another primate malaria species carried by macaques [76,77,78]. LULCC, resulting in increased spatial overlap between people, macaques and mosquitoes, likely drive this emergence [58, 79, 80]. In Northern Sabah, Malaysia, village-level P. knowlesi incidence was positively associated with both forest cover and historical forest loss, with wider community exposure associated with forest fragmentation and agricultural practices [81, 82]. Deforestation is also associated with changes in macaque movements and increased contact between people and mosquito vectors at forest edges [83, 84].

Similarly, within the South American rainforests, a human infection with the simian malaria P. simium had been historically reported, although there was little evidence of widespread human infections until recently [53]. Since 1993, sporadic human cases of a P. vivax- like malaria infection were reported from the Atlantic forest region of Rio de Janeiro, Brazil, an area in which malaria had previously been eliminated. Parasitological and molecular investigations of these infections revealed human cases of P. simium, including 28 confirmed cases in 20152016 [85]. Naturally acquired human infections with the simian malaria Plasmodium brasilianum were confirmed in indigenous communities in the Venezuelan Amazon [86]. The increasing incidence and widespread circulation of these zoonotic malaria species poses significant threats to malaria eradication, highlighting the need to understand how risks evolve with future LULCC.

These rapidly changing landscapes have huge potential to undermine any future malaria eradication efforts. While increasing development, urbanization and expanded healthcare coverage are widely expected to reduce malaria risks globally [4], these trends also drive the increased needs for resources underlying most LULCC. Further, these changes exert increasing evolutionary pressures on ecological systems to adapt to changing environments. For example, while malaria is historically a predominantly rural disease in Africa, the urban malaria vector An. stephensi typically found in India has invaded areas of East Africa, largely driven by truck routes and trade [87, 88]. Malaria control and eradication strategies need to detect and adjust to changing epidemiological patterns. While LULCC impacts on socio-ecological systems driving malaria transmission are complex, priorities for malaria eradication strategies are outlined, highlighting the need for engagement across different sectors.

One of the key lessons learnt from the previous malaria eradication failures is the need for context-specific national malaria elimination strategies with the flexibility to adjust to short and long term changes [4]. Highly effective control strategies in one context may be ineffective in other areas, for example, the limited utility of bed nets and indoor residual spraying in areas where transmission is driven by exophagic mosquito species and outdoor occupational activities [89]. A large volume of literature addresses this need to stratify approaches to malaria control and defines malaria paradigms, characteristics of ecosystems and populations relevant to control [90]. While this recognizes the heterogeneity of malaria transmission, higher levels of granularity in social and ecological factors are needed to accurately monitor and control malaria risks. For example, widely described forest malaria in Southeast Asia encompasses a range of transmission patterns, from hunting in deep forest environments to occupational risks at industrial rubber plantations to peri-domestic exposure around secondary forest edges near households [36, 83, 91]. These differences have critical implications for identifying populations at risk and effective interventions, requiring continued engagement of local control programmes and experts to design context-specific control measures.

Estimating the impacts of LULCC also requires understanding the wider socioeconomic and environmental contexts in which these changes occur. Primarily driven by economic forces, increased prosperity from LULCC can reduce malaria burdens despite ecological changes favourable to transmission [45]. Conversely, economic pressures driving LULCC can simultaneously weaken health systems and amplify ecological impacts. Within Venezuela, economic collapses and political instability have both crippled malaria control programmes and driven rapid deforestation due to migration to frontier areas for extractive activities [92, 93]. Changes to vector habitats and accompanying increases in vulnerability of human populations lead to a massive resurgence of malaria despite elimination of malaria within large regions of Venezuela in 1961 [94]. Venezuela now accounts for a substantial percentage of malaria within the Americas, threatening elimination and control programmes in surrounding countries [95]. Similarly, LULCC interacts with wider climate changes, either increasing or decreasing vulnerability to climate anomalies or longer-term changes.

Because of these interactions, associations between LULCC and malaria risks are modulated by the spatial and temporal scales of analysis. Initial LULCC impacts on disease transmission from disruption of existing ecosystems may change over time as transmission reaches new equilibrium states. Following deforestation, subsequent stages of forest succession and agricultural development may either create new habitats for disease vectors and hosts or lead to overall decreases in malaria burdens [7]. Ecological processes affecting the distribution of people, disease vectors and wildlife hosts may occur at highly local to larger regional scales [96]. For other vector-borne diseases, variations in host richness and ecological community structure have been shown to be important at a fine spatial scale while changes in climate and other abiotic factors are more important across larger scales [97].

Monitoring these changes in malaria transmission requires detailed data on malaria infection and disease burden, human, mosquito and other host distributions and wider environmental factors collected in consistent ways across the relevant scales. The WHO now recognizes surveillance as a core intervention required to achieve malaria elimination. However, despite efforts to digitize and geolocate malaria surveillance data and advances in using climate data to inform malaria early warning systems [98], LULCC data rarely informs malaria surveillance.

New sources of Earth Observation data offer unprecedented opportunities to detect changes in land cover and proactively target surveillance and control measures. Earth Observation data is widely used to monitor physical changes to the environment such as land cover and surface water changes; this data can be used to quantify extents of land cover changes as well as to characterize habitat configuration, such as levels of fragmentation and proximity of forests to households. High-resolution satellite imagery is freely available through governmental and international agencies such as NASA (https://eospso.nasa.gov/) and the European Space Agency (https://www.esa.int/ESA) with many countries additionally maintaining their own dedicated satellites. While health programmes can be limited by the technical, software and time required to process this data into a usable form, cloud-based computing platforms such as Earth on Amazon Web Services (https://aws.amazon.com/earth/) and Google Earth Engine (https://earthengine.google.com/) provide access to imagery and infrastructure to analyse planetary-level data. Additional online platforms, such as Global Forest Watch, publish processed data of forest cover and forest loss online in addition to near real-time deforestation mobile alerts designed to provide actionable information to government agencies [99]. Low-cost drones (unmanned aerial vehicles or UAVs) have also been utilized by malaria programmes in diverse ecological contexts including Malaysia, Tanzania and Peru [100,101,102]. Drones allow collection of fine-scale data at user-defined intervals and can be used to monitor deforestation, agriculture and development (Fig.4). Despite the increasing accessibility of Earth Observation and spatial data, these are rarely used by health programmes and further work is needed to develop capacity to integrate these data within surveillance systems.

Examples of remote sensing data on landcover: a. very high-resolution data collected by UAV (11cm per pixel) in Malaysian Borneo; b. false colour composite from LANDSAT satellite data of Lake Victoria in Uganda (30m per pixel)

Malaria risk models have incorporated land use factors to develop spatially and/or temporal predictions of malaria risks, potentially allowing targeting of interventions and strategic planning [103]. Within research communities, datasets on land cover, land use and associated characteristics (such as vegetation indices or land surface temperatures) are widely used to identify areas with increased risk [104,105,106,107,108]. Data on landscapes and mosquito can be integrated with detailed behavioural and demographic risk determinants to explore plausible land use change scenarios and impacts on human health [109]. However, despite increasing use in scientific literature, there are fewer examples of LULCC data directly informing malaria surveillance programmes. Notably, Malaysia incorporates metrics of recent deforestation and recent construction activities into malaria foci investigations, defining receptivity based on numerous ecological and social factors [110]. More broadly, global planetary health projects have also highlighted the need to link both health and environmental data to monitor changing risks [111]. Major advances in computing, information technologies and environmental monitoring have tremendous potential to improve malaria surveillance and are a priority for future research and development.

Ultimately, achieving malaria eradication requires not only monitoring and responding to impacts of LULCC on malaria transmission but actively mitigating risks within future landscapes. Agriculture covers over 37% of global land surfaces, 50 million km2 globally [112]. These landscapes are entirely man-made, providing opportunities to design malaria resistant environments. Approaches to reduce malaria transmission within these landscapes generally comprise of three approaches: environmental modification on land, water or vegetation with long-lasting effects for vector habitat reduction; environmental manipulation that generates unfavourable temporary conditions for vectors; and modification of human habitation to reduce exposure to vectors.

A systematic review identified 16 studies that applied environmental modification and 8 studies that modified human habitation, reducing the risk ratio of malaria by 88% and 79.5%, respectively [113]. For example, cacao plantations under nurse trees in Trinidad generated ideal breeding sites within epiphytic bromeliads for Anopheles bellator, the main local malaria vector. Control of the resulting malaria epidemic was achieved through environmental manipulation with the modification of plantation techniques [28]. With the intent of preventing malaria epidemics, environmental manipulation has been proposed in Panama and other Latin American countries by increasing forest cover recovery in highly disturbed deforested areas, thus favouring the prevalence of auxiliary over primary vectors [34]. Malaria vector breeding sites can also be decreased through effective water management, mitigating potential effects of irrigation or dams. Utilization of intermittent irrigation in African rice fields has greatly reduced anopheline densities and increased rice yields while construction of several types of siphons and small dams in Sri Lanka and Malaysias rivers and streams eliminated mosquito breeding habitats. Environmental management interventions in the reservoirs of the Tennessee River Valley including an integrated operating rule for water fluctuation cycles, reduced Anopheles breeding sites significantly [113].

One of the most successful large-scale environmental modification interventions was during the construction of the Panama Canal. In 1878, this construction was halted due to engineering challenges, yellow fever and malaria and the resulting deaths amongst workers. Sanitation improvements allowed continuation of the project, including implementation of temporary and permanent drainage infrastructure and vegetation management, while dramatically decreasing malaria incidence [113]. More recently, plans for major developments have included evaluation of impacts on malaria transmission and preventive measures to mitigate these. For example, during the plans for Batu Hijau, a large-scale surface mine in Indonesia, environmental assessments highlighted impacts on community malaria risks, particularly in relation to lagoons and potential vector breeding sites. This prompted the establishment of a corporate public health programme focussing on environmental management, larvicides, mosquito control and active and passive detection and treatment of malaria cases [114]. Similarly, health programmes were incorporated into projects led by ExxonMobil in Papua New Guinea and hydroelectric projects in Lao PDR to address negative externalities of developments and present templates for future developments [114].

The impacts of LULCC on malaria transmission are highly complex and context specific; environmental and demographic changes within a specific setting may lead to increases or decreases in malaria risks. Impacts may vary over space and time due to interactions between the environment and intrinsic factors such as species composition and ecology, demographic changes influencing socioeconomic status, risk behaviours and access to control measures. Malaria eradication will not be possible without accounting for these changing risks. This requires engaging with partners outside the health sector to develop interventions appropriate to local socio-ecological contexts, integrate environmental data into malaria surveillance systems and engineer malaria resistant landscapes.

All data is publicly available. Full versions of World Health Organization reports and policies are available at https://doi.org/10.5281/zenodo.3753145 and https://www.who.int/publications/i/item/malaria-eradication-benefits-future-scenarios-feasibility.

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This work was partially funded by the World Health Organization under the Strategic Advisory Group for Malaria Eradication. Additional funding support was provided by the CGIAR Research Programme on Agriculture for Nutrition and Health (A4NH; https://a4nh.cgiar.org/). The opinions expressed here belong to the authors and do not necessarily reflect those of A4NH or CGIAR.

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