Bioenergetic challenges of microbial iron metabolisms
2011; Elsevier BV; Volume: 19; Issue: 7 Linguagem: Inglês
10.1016/j.tim.2011.05.001
ISSN1878-4380
AutoresLina J. Bird, Violaine Bonnefoy, Dianne K. Newman,
Tópico(s)Geochemistry and Elemental Analysis
ResumoBefore cyanobacteria invented oxygenic photosynthesis and O2 and H2O began to cycle between respiration and photosynthesis, redox cycles between other elements were used to sustain microbial metabolism on a global scale. Today these cycles continue to occur in more specialized niches. In this review we focus on the bioenergetic aspects of one of these cycles – the iron cycle – because iron presents unique and fascinating challenges for cells that use it for energy. Although iron is an important nutrient for nearly all life forms, we restrict our discussion to energy-yielding pathways that use ferrous iron [Fe(II)] as an electron donor or ferric iron [Fe(III)] as an electron acceptor. We briefly review general concepts in bioenergetics, focusing on what is known about the mechanisms of electron transfer in Fe(II)-oxidizing and Fe(III)-reducing bacteria, and highlight aspects of their bioenergetic pathways that are poorly understood. Before cyanobacteria invented oxygenic photosynthesis and O2 and H2O began to cycle between respiration and photosynthesis, redox cycles between other elements were used to sustain microbial metabolism on a global scale. Today these cycles continue to occur in more specialized niches. In this review we focus on the bioenergetic aspects of one of these cycles – the iron cycle – because iron presents unique and fascinating challenges for cells that use it for energy. Although iron is an important nutrient for nearly all life forms, we restrict our discussion to energy-yielding pathways that use ferrous iron [Fe(II)] as an electron donor or ferric iron [Fe(III)] as an electron acceptor. We briefly review general concepts in bioenergetics, focusing on what is known about the mechanisms of electron transfer in Fe(II)-oxidizing and Fe(III)-reducing bacteria, and highlight aspects of their bioenergetic pathways that are poorly understood. Billions of years ago, microbial iron metabolisms probably drove the carbon cycle and catalyzed the global deposition of massive sedimentary ore deposits known as banded iron formations [1Canfield D.E. et al.Early anaerobic metabolisms.Philos. Trans. R. Soc. B: Biol. Sci. 2006; 361: 1819-1834Crossref PubMed Scopus (252) Google Scholar]. Today, these microbial metabolisms remain highly relevant in a variety of environments, ranging from anaerobic aquifers [2Lovley D.R. Dissimilatory Fe(III) and Mn(IV) reduction.Microbiol. Rev. 1991; 55: 259-287PubMed Google Scholar] and acid mines [3Baker B.J. Banfield J.F. Microbial communities in acid mine drainage.FEMS Microbiol. Ecol. 2003; 44: 139-152Crossref PubMed Scopus (825) Google Scholar] to the deep sea [4Edwards K.J. et al.Geomicrobiology of the ocean crust: a role for chemoautotrophic Fe-bacteria.Biol. Bull. 2003; 204: 180-185Crossref PubMed Scopus (58) Google Scholar]. Because of the importance of these organisms to modern biogeochemical cycles, and their potential usefulness in bioremediation and biotechnology, a number of informative reviews have been written on their ecology, physiology and diversity [5Croal L.R. et al.The genetics of geochemistry.Annu. Rev. Genet. 2004; 38: 175-202Crossref PubMed Scopus (70) Google Scholar, 6Richardson D.J. Bacterial respiration: a flexible process for a changing environment.Microbiology. 2000; 146: 551-571Crossref PubMed Scopus (290) Google Scholar, 7Shi L. et al.The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer.Environ. Microbiol. Rep. 2009; 1: 220-227Crossref PubMed Scopus (235) Google Scholar, 8Weber K. et al.Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction.Nat. Rev. Microbiol. 2006; 4: 752-764Crossref PubMed Scopus (1135) Google Scholar, 9Lovley D.R. et al.Dissimilatory Fe(III) and Mn(IV) reduction.Adv. Microb. 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Acta. 2008; 1777: 1471-1479Crossref PubMed Scopus (43) Google Scholar], relatively little attention has been paid to the bioenergetic underpinnings of these metabolisms, and these are the focus of this review. Electron-transfer metabolisms allow organisms to capture, store, and release energy (Box 1). Not only do these metabolisms impact profoundly upon the environments in which they occur, they are also fascinating at the molecular level. Substrates that are oxidized (give up electrons) are termed electron donors (i.e. reductants); substrates that are reduced (gain electrons) are termed electron acceptors (i.e. oxidants). It is well known that oxygenic phototrophs, such as plants, harvest energy from the sun by transferring electrons from H2O to CO2, producing O2 and reduced carbon compounds – sugars, fats, proteins, DNA, and numerous small metabolites. The details of this remarkable bioenergetic feat have been studied for decades, and much is now understood about how water is oxidized by the photosynthetic reaction center [15Allen J.P. Williams J.C. The evolutionary pathway from anoxygenic to oxygenic photosynthesis examined by comparison of the properties of photosystem II and bacterial reaction centers.Photosynth. Res. 2011; 107: 59-69Crossref PubMed Scopus (27) Google Scholar] and the path electrons take to fix CO2 [16White D. The Physiology and Biochemistry of Prokaryotes.3rd edn. Oxford University Press, 2007Google Scholar, 17Calvin M. The path of carbon in photosynthesis.Nobel Lectures, Chemistry 1942–1962. Elsevier Publishing Company, 1961Google Scholar]. Similarly, it is well appreciated that heterotrophs, such as animals, can obtain energy by oxidizing organic material to CO2 and transferring electrons to O2 to make H2O; mechanistic studies of the respiratory electron-transport chain date back nearly a century [18Mitchell P. David Keilin's respiratory chain concept and its chemiosmotic consequences.in: Forsen S. Nobel Lectures in Chemistry 1971–1980. World Scientific Publishing Company, 1978Google Scholar]. Although important details regarding electron transport in oxygenic photosynthesis and aerobic respiration remain unknown, it is fair to say that the depth of understanding of these systems is orders of magnitude greater than that of bioenergetic pathways involving iron.Box 1Iron chemistryThe state of iron in the environment depends on many factors, including pH, Eh, and the presence of complexing agents. The midpoint potential (Em) of Fe2+/Fe3+, in the absence of precipitation (which only occurs at pH < 3), is about 0.77 V. At pH > 3, the formation of a solid effectively removes Fe(III) from solution, making iron oxidation more favorable (lowering Em). The amount that the reduction potential is lowered depends on the solubility of the mineral formed. Iron hydroxide [Fe(OH)3], for example, is poorly crystalline and more soluble than ordered minerals such as hematite (Fe2O3). The potential of Fe(OH)3/Fe(II) is therefore significantly higher than that of, for example, Fe2O3/Fe(II) because hematite is a less soluble mineral. Chelators can lower or raise the reduction potential depending on their properties. Citrate and nitrilotriacetic acid (NTA), for example, bind more tightly to Fe(III) and stabilize it, thus lowering the reduction potential [69Stumm W. Morgan J.J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters.3rd edn. Wiley, 1996Google Scholar]. Other chelators bind more tightly to Fe(II) thus raising the reduction potential. Some of the potentials relevant to this review are listed in Table 1.It is important to note that, although this review deals primarily with thermodynamic constraints on microbial iron metabolisms, not everything can be explained from a thermodynamic perspective. This is because metabolic reactions must not only be thermodynamically favorable, but kinetically favorable as well. Abiotic oxidation must proceed slowly enough that microorganisms can take advantage of the reaction; at the same time, the iron must be in a form that is accessible to the microorganisms. Several studies have shown that rates of Fe(III) reduction by microorganisms depend on the solubility of iron minerals [70Bonneville S. et al.Solubility and dissimilatory reduction kinetics of iron(III) oxyhydroxides: a linear free energy relationship.Geochim. Cosmochim. Acta. 2009; 73: 5273-5282Crossref Scopus (130) Google Scholar] or the affinity of the ferric chelator [71Haas J.R. Dichristina T.J. Effects of Fe(III) chemical speciation on dissimilatory Fe(III) reduction by Shewanella putrefaciens.Environ. Sci. Technol. 2002; 36: 373-380Crossref PubMed Scopus (67) Google Scholar]. Understanding iron metabolisms in the environment thus requires a grasp of both thermodynamics and kinetics. Finally, random quirks of evolution ultimately dictate what is possible or not: even if a substrate is thermodynamically and kinetically favorable, an organism must possess the machinery required to recognize it. The state of iron in the environment depends on many factors, including pH, Eh, and the presence of complexing agents. The midpoint potential (Em) of Fe2+/Fe3+, in the absence of precipitation (which only occurs at pH < 3), is about 0.77 V. At pH > 3, the formation of a solid effectively removes Fe(III) from solution, making iron oxidation more favorable (lowering Em). The amount that the reduction potential is lowered depends on the solubility of the mineral formed. Iron hydroxide [Fe(OH)3], for example, is poorly crystalline and more soluble than ordered minerals such as hematite (Fe2O3). The potential of Fe(OH)3/Fe(II) is therefore significantly higher than that of, for example, Fe2O3/Fe(II) because hematite is a less soluble mineral. Chelators can lower or raise the reduction potential depending on their properties. Citrate and nitrilotriacetic acid (NTA), for example, bind more tightly to Fe(III) and stabilize it, thus lowering the reduction potential [69Stumm W. Morgan J.J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters.3rd edn. Wiley, 1996Google Scholar]. Other chelators bind more tightly to Fe(II) thus raising the reduction potential. Some of the potentials relevant to this review are listed in Table 1. It is important to note that, although this review deals primarily with thermodynamic constraints on microbial iron metabolisms, not everything can be explained from a thermodynamic perspective. This is because metabolic reactions must not only be thermodynamically favorable, but kinetically favorable as well. Abiotic oxidation must proceed slowly enough that microorganisms can take advantage of the reaction; at the same time, the iron must be in a form that is accessible to the microorganisms. Several studies have shown that rates of Fe(III) reduction by microorganisms depend on the solubility of iron minerals [70Bonneville S. et al.Solubility and dissimilatory reduction kinetics of iron(III) oxyhydroxides: a linear free energy relationship.Geochim. Cosmochim. Acta. 2009; 73: 5273-5282Crossref Scopus (130) Google Scholar] or the affinity of the ferric chelator [71Haas J.R. Dichristina T.J. Effects of Fe(III) chemical speciation on dissimilatory Fe(III) reduction by Shewanella putrefaciens.Environ. Sci. Technol. 2002; 36: 373-380Crossref PubMed Scopus (67) Google Scholar]. Understanding iron metabolisms in the environment thus requires a grasp of both thermodynamics and kinetics. Finally, random quirks of evolution ultimately dictate what is possible or not: even if a substrate is thermodynamically and kinetically favorable, an organism must possess the machinery required to recognize it. One of the most exciting traits of bacteria and archaea is their ability to extract energy from sources that are inaccessible to other life forms. A minimal constraint for any catabolic (i.e. energy-yielding) pathway is the generation of a proton motive force (PMF) across the cytoplasmic membrane that can be harnessed to synthesize ATP, energize membrane transporters, and drive flagellar rotation. Microbes have diverse ways of doing this, ranging from using coupling sites in the electron transport chain to running the ATP synthase in reverse [16White D. The Physiology and Biochemistry of Prokaryotes.3rd edn. Oxford University Press, 2007Google Scholar]. Nowhere is this better exemplified than in the case of microbial iron metabolisms. For example, instead of obtaining electrons from water as described above, some photosynthetic bacteria oxidize Fe(II) to fuel CO2 fixation (anoxygenic photosynthesis); other bacteria transfer electrons from organic carbon to Fe(III) instead of to O2 (heterotrophic respiration or fermentation); still others obtain energy by oxidizing Fe(II) and reducing O2 or NO3 (lithotrophic respiration). Although the general principles of energy conservation are the same, the mechanisms vary. Knowledge of what controls microbial iron metabolisms at a cellular scale is necessary to predict their impact in bioremediation and mining environments. Moreover, there is currently much interest in biofuel cells that use bacteria to generate electricity or other forms of fuel. In many cases, the systems that bacteria use to transfer electrons to and from electrodes are the same ones that they use to grow on solid substrates, such as iron minerals [19Bretschger O. et al.Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants.Appl. Environ. Microbiol. 2007; 73: 7003-7012Crossref PubMed Scopus (424) Google Scholar]. Understanding the mechanisms of these systems is vital if we wish to optimize them for the production of electricity or fuel. In the following sections we review what is understood about: (i) coupling Fe(II) oxidation to O2 reduction at acidic pH, (ii) coupling Fe(II) oxidation to CO2 reduction in photosynthesis, and (iii) coupling Fe(III) reduction to organic carbon oxidation. Fe(II) oxidation is performed by many different types of bacteria, including autotrophs and heterotrophs, phototrophs and chemotrophs, and aerobes and anaerobes. Because Fe(II) oxidizes rapidly in the presence of O2 at neutral pH, Fe(II)-oxidizing bacteria are limited to environments with low (or no) O2 or to highly acidic environments where abiotic oxidation is much slower. Lithotrophic iron oxidizers obtain energy by coupling Fe(II) oxidation to the reduction of a compound with a more positive reduction potential. For acidophiles – microorganisms living at acidic pH – this terminal electron acceptor is O2. There are some advantages to acidophilic Fe(II) oxidation. The main benefit is that Fe(II) autooxidation by O2 is minimized, rendering Fe(II) stable and readily available as an electron donor for bioenergetic processes. Interestingly, whereas the natural substrates for most of the acidophilic iron oxidizers are minerals, such as pyrite (FeS2) or chalcopyrite (CuFeS2), these Fe(II) minerals are considerably more soluble than Fe(III) (hydro)oxides, thus acidophiles probably encounter Fe2+ as their substrate. Another advantage is that the midpoint potential (Em) of the O2/H2O couple increases at low pH, increasing the potential energy available from Fe(II) oxidation (see below). However, Fe(II)-oxidizing acidophiles face several specific challenges as described below. General challenges of acidophily. Several reviews on pH homeostasis in acidophiles have been published [20Matin A. Keeping a neutral cytoplasm; the bioenergetics of obligate acidophiles.FEMS Microbiol. Rev. 1990; 75: 307-318Crossref Google Scholar, 21Baker-Austin C. Dopson M. Life in acid: pH homeostasis in acidophiles.Trends Microbiol. 2007; 15: 165-171Abstract Full Text Full Text PDF PubMed Scopus (359) Google Scholar, 22Dopson, M. (2011) Ecology, adaptations, and applications of acidophiles. In Extremophiles: Microbiology and Biotechnology (Anitori, R., ed.), Horizon Press (in press)Google Scholar, 23Slonczewski J.L. et al.Cytoplasmic pH measurement and homeostasis in bacteria and archaea.Adv. Microb. Physiol. 2009; 55 (1–79, 317)PubMed Google Scholar, 24Cox J.C. et al.Transmembrane electrical potential and transmembrane pH gradient in the acidophile Thiobacillus ferrooxidans.Biochem. J. 1979; 178: 195-200Crossref PubMed Scopus (69) Google Scholar]. Briefly, acidophiles maintain circumneutral cytoplasmic pH by maintaining an inverted transmembrane electrical potential, ΔΨ (positive inside). The external medium acidity provides a large favorable chemical potential of protons (H+) between the periplasm and cytoplasm, ΔpH. Protons enter the cytoplasm through leakage, secondary H+ pumps, or via H+-translocating ATP synthases (thereby generating ATP). The PMF is created by the topography of the electron transport chain components and is maintained by the removal of cytoplasmic H+ by the reduction of O2 to H2O. Specific challenges of iron oxidation. In the neutral pH of the cytoplasm, Fe(II) is rapidly autooxidized, producing free radicals that damage macromolecules, leading to cell death. Furthermore, the Fe(III) produced will clog and acidify the cytoplasm through ferric oxyhydroxide precipitation. Acidophilic Fe(II)-oxidizing bacteria appear to avoid these problems by oxidizing Fe(II) outside the cell. Energetics of Fe(II) oxidation. The Em of Fe(II)/Fe(III) is about +0.77 V whereas O2/H2O is +0.82 V at neutral pH. However, the involvement of H+ in O2 reduction (Equation 1) confers pH dependence to the Em of the O2/H2O couple, which increases to +1.12 V at pH 2, making more energy available (Figure 1) [25Ingledew W.J. Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph.Biochim. Biophys. Acta. 1982; 683: 89-117Crossref PubMed Scopus (294) Google Scholar].2e− + 1/2O2 + 2H+ → H2O(1) The localization of the O2 reduction site near the periplasmic face of the membrane where the local environment is acidic allows the Em of O2/H2O to be increased, even though the H+ used in the reaction comes from the neutral cytoplasm. Fe(II)-oxidizing autotrophs obtain both energy and reducing power from Fe(II) oxidation to fix CO2 and, if necessary, N2. Fe(II) oxidation must therefore provide not only ATP but also reduced NAD+. Because the Em of NAD+/NADH is –0.32 V at cytoplasmic pH, some electrons coming from Fe(II) oxidation are pushed ‘uphill’ against the unfavorable redox potential (Figure 1). This ‘reverse’ electron transport is driven by the PMF [14Ferguson S.J. Ingledew W.J. Energetic problems faced by micro-organisms growing or surviving on parsimonious energy sources and at acidic pH: I. Acidithiobacillus ferrooxidans as a paradigm.Biochim. Biophys. Acta. 2008; 1777: 1471-1479Crossref PubMed Scopus (43) Google Scholar, 25Ingledew W.J. Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph.Biochim. Biophys. Acta. 1982; 683: 89-117Crossref PubMed Scopus (294) Google Scholar]. Although this electron pathway has been described in the Gram-negative bacterium Acidithiobacillus ferrooxidans (see below), how the electron flow switches between O2 and NAD+ is not understood [14Ferguson S.J. Ingledew W.J. Energetic problems faced by micro-organisms growing or surviving on parsimonious energy sources and at acidic pH: I. Acidithiobacillus ferrooxidans as a paradigm.Biochim. Biophys. Acta. 2008; 1777: 1471-1479Crossref PubMed Scopus (43) Google Scholar]. Electron pathway from Fe(II) to O2 in At. ferrooxidans. The electron transfer chain between Fe(II) and O2 was first proposed [25Ingledew W.J. Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph.Biochim. Biophys. Acta. 1982; 683: 89-117Crossref PubMed Scopus (294) Google Scholar] and investigated [26Appia-Ayme C. et al.Characterization of an operon encoding two c-type cytochromes, an aa(3)-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020.Appl. Environ. Microbiol. 1999; 65: 4781-4787Crossref PubMed Google Scholar] in At. ferrooxidans. It has since been extensively studied ([27Bonnefoy V. Bioinformatics and genomics of iron- and sulfur- oxidizing acidophiles.in: Barton L.L. Geomicrobiology: Molecular and Environmental Perspective. Springer, 2010: 169-192Crossref Scopus (17) Google Scholar, 28Holmes D. Bonnefoy V. Genetic and bioinformatic insights into iron and sulfur oxidation mechanisms of bioleaching organisms.in: Rawlings D.E. Johnson D.B. Biomining. 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This wire consists of the outer-membrane cytochrome c-type protein Cyc2, the periplasmic blue copper protein rusticyanin, the membrane-bound cytochrome c4 Cyc1, and the integral cytoplasmic-membrane cytochrome oxidase CoxBACD, where O2 is reduced to H2O (Figure 1). Proton translocation through the oxidase combined with the consumption of protons by the cytoplasmic reduction of O2 helps the cell to maintain a large difference in proton concentration between the cytoplasm (pH 6.5) and the periplasm (pH 2). Driven by the PMF, protons enter the cytoplasm through the ATP synthase and also through membrane-associated transport processes such as the antiport or symport of solutes and the efflux or influx of metal(oid)s. The PMF is also thought to provide the energy to push the electrons ‘uphill’ to NAD+. In this pathway electrons are transferred from rusticyanin via the cytochrome c4 CycA1, the cytochrome bc1 complex, and the membrane-associated quinones to the NADH dehydrogenase (NADH1) complex. The split of electron flow to NAD+ (‘uphill’) or O2 (‘downhill’) has been proposed to occur at the rusticyanin level. By adjusting the electron flow at the rusticyanin branch point, At. ferrooxidans could balance NAD+ and O2 reduction. Fe(II) oxidation in other acidophiles. The Fe(II) oxidation pathways of some other acidophiles have been proposed, mainly from functional genomics data. These pathways have been reviewed recently ([27Bonnefoy V. Bioinformatics and genomics of iron- and sulfur- oxidizing acidophiles.in: Barton L.L. Geomicrobiology: Molecular and Environmental Perspective. Springer, 2010: 169-192Crossref Scopus (17) Google Scholar, 28Holmes D. Bonnefoy V. Genetic and bioinformatic insights into iron and sulfur oxidation mechanisms of bioleaching organisms.in: Rawlings D.E. Johnson D.B. Biomining. Springer-Verlag, 2007: 281-307Crossref Scopus (53) Google Scholar] and references therein). The various organisms differ in the components involved, even between phylogenetically related species [31Barr D.W. et al.Respiratory chain components of iron-oxidizing, acidophilic bacteria.FEMS Microbiol. Lett. 1990; 70: 85-90Crossref Google Scholar, 32Blake 2nd, R.C. et al.Respiratory components in acidophilic bacteria that respire on iron.Geomicrobiol. J. 1992; 10: 173-192Crossref Scopus (39) Google Scholar, 33Blake 2nd, R.C. et al.Enzymes of aerobic respiration on iron.FEMS Microbiol. Rev. 1993; 11: 9-18Crossref PubMed Scopus (73) Google Scholar, 34Amouric A. et al.Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways.Microbiology. 2011; 157: 111-122Crossref PubMed Scopus (89) Google Scholar]. However, although the components of the pathway might differ significantly, the bioenergetics of the different systems are presumed to be similar (at least in Gram-negative bacteria) – they all conserve energy by transferring electrons from Fe(II) to O2 through an outer membrane cytochrome c, a periplasmic protein, a membrane-bound cytochrome c and an integral cytoplasmic-membrane terminal oxidase; in addition, they pump electrons ‘uphill’ to NAD+ through a bc1 complex. Fe(II) oxidation can supply electrons to fix CO2 in anoxygenic photosynthesis according to the general reaction [35Jiao Y. Newman D.K. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1.J. Bacteriol. 2007; 189: 1765-1773Crossref PubMed Scopus (153) Google Scholar] given in Equation 2.4Fe2+ + CO2 + 11H2O + hv → [CH2O] + 4Fe(OH)3 + 8H+(2) Phototrophic Fe(II) oxidation was first postulated by Hartman [36Hartman H. The evolution of photosynthesis and microbial mats: A speculation on the banded iron formations.in: Chohen Y. Microbial Mats: Stromatolites. A.R. Liss, 1984: 449-453Google Scholar] and was first described in purple nonsulfur bacteria in 1993 [37Widdel F. et al.Ferrous iron oxidation by anoxygenic phototrophic bacteria.Nature. 1993; 362: 834-836Crossref Scopus (546) Google Scholar]. Several other Fe(II)-oxidizing purple sulfur and nonsulfur bacteria and one green sulfur bacterium have since been isolated [35Jiao Y. Newman D.K. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1.J. Bacteriol. 2007; 189: 1765-1773Crossref PubMed Scopus (153) Google Scholar, 38Ehrenreich A. Widdel F. Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism.Appl. Environ. Microbiol. 1994; 60: 4517-4526PubMed Google Scholar, 39Heising S. Schink B. Phototrophic oxidation of ferrous iron by a Rhodomicrobium vannielii strain.Microbiology. 1998; 144: 2263-2269Crossref PubMed Scopus (78) Google Scholar, 40Jiao Y. et al.Isolation and characterization of a genetically tractable photoautotrophic Fe(II)-oxidizing bacterium, Rhodopseudomonas palustris strain TIE-1.Appl. Environ. Microbiol. 2005; 71: 4487-4496Crossref PubMed Scopus (150) Google Scholar, 41Croal L.R. et al.Iron isotope fractionation by Fe(II)-oxidizing photoautotrophic bacteria.Geochim. Cosmochim. Acta. 2004; 68: 1227-1242Crossref Scopus (276) Google Scholar, 42Heising S. et al.Chlorobium ferrooxidans sp nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a ‘Geospirillum’ sp. strain.Arch. Microbiol. 1999; 172: 116-124Crossref PubMed Scopus (156) Google Scholar]. These bacteria all live at circumneutral pH. Challenges of photosynthetic Fe(II) oxidation. Similar to their acidophilic counterparts, photosynthetic iron-oxidizing bacteria face several challenges: (i) they must be able to oxidize the various forms of Fe(II) found at circumneutral pH, including free ions, ligand-bound Fe(II), and Fe(II) that is trapped in minerals, all of which have widely varying reduction potentials (Table 1); (ii) they must transfer electrons uphill to NAD+; and (iii) they must deal with the product of Fe(II) oxidation, Fe(III), which precipitates rapidly as ferric (hydr)oxide [Fe(OH)3] at pH 7. Although genes catalyzing phototrophic Fe(II) oxidation have been identified in two purple nonsulfur bacteria, the details of how their protein products function are poorly understood. No studies have yet described the genes or gene products involved in Fe(II) oxidation by green sulfur bacteria, but it is reasonable to assume that they will be different from those in purple bacteria because their photosynthetic reaction centers are significantly different.Table 1Reduction potentials and free energies of relevant compounds and proteinsReduction pairEenv* (volts)aEenv* indicates environmentally relevant midpoint potentials: pH 7 except where noted, standard concentrations except for solid Fe minerals, for which Fe2+ is 100μM.ΔG (kJ/mol)bΔG calculations assume standard conditions and pH 7, except in the case of iron minerals where [Fe2+] is assumed to be 100μM.RefsTerminal electron acceptorsFe3+/Fe2+ (pH 2)+0.77–74.274Thamdrup B. Bacterial manganese and iron reduction in aquatic sediments.Adv. Microb. Ecol. 2000; 16: 41-84Crossref Scopus (491) Google ScholarFe(III)-citrate/Fe(II)-citrate+0.385–37.174Thamdrup B. Bacterial manganese and iron reduction in aquatic sediments.Adv. Microb. Ecol. 2000; 16: 41-84Crossref Scopus (491) Google ScholarFe(III)-NTA/Fe(II)-NTA+0.372–35.974Thamdrup B. Bacterial manganese and iron reduction in aquatic sediments.Adv. Microb. Ecol. 2000; 16: 41-84Crossref Scopus (491) Google ScholarFerrihydritesolid/Fe2++0.1 to –0.1–9.6 to 9.674Thamdrup B. Bacterial manganese and iron reduction in aquatic sediments.Adv. Microb. Ecol. 2000; 16: 41-84Crossref Scopus (491) Google Scholarα-FeOOHsolid/Fe2+–0.27426.474Thamdrup B. Bacterial manganese and iron reduction in aquatic sediments.Adv. Microb. Ecol. 2000; 16: 41-84Crossref Scopus (491) Google Scholarα-Fe2O3solid/Fe2+–0.2
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