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The Interplay of Microbially Mediated and Abiotic Reactions in the Biogeochemical Fe Cycle

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The Interplay of Microbially Mediated and Abiotic Reactions in the Biogeochemical Fe Cycle REVIEWS The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle Emily D. Melton, Elizabeth D. Swanner, Sebastian Behrens, Caroline Schmidt and Andreas Kappler Abstract | Many iron (Fe) redox processes that were previously assumed to be purely abiotic, such as photochemical Fe reactions, are now known to also be microbially mediated. Owing to this overlap, discerning whether biotic or abiotic processes control Fe redox chemistry is a major challenge for geomicrobiologists and biogeochemists alike. Therefore, to understand the network of reactions within the biogeochemical Fe cycle, it is necessary to determine which abiotic or microbially mediated reactions are dominant under various environmental conditions. In this Review, we discuss the major microbially mediated and abiotic reactions in the biogeochemical Fe cycle and provide an integrated overview of biotic and chemically mediated redox transformations. Fe speciation The environmental abundance of iron (Fe) and its pos‑ and temporal distribution of Fe redox species in some Refers to the redox state of session of electrons in d orbitals with π‑character, which environments, such as heterogeneous sediments, plant iron (Fe) and the identity of its can form complexes with carbon (C), oxygen (O), nitro‑ rhizospheres and microbial mats6, and abiotic Fe trans‑ ligands. The two most common gen (N) and sulphur (S) species, make it an essential ele‑ formations with biologically produced intermediates environmental Fe redox ment for nearly all living organisms. Fe occurs in two must be taken into account7,8. species are Fe(II) and Fe(III). main redox states in the environment: oxidized ferric Fe Despite our growing knowledge of the wide‑ (Fe(iii)), which is poorly soluble at circumneutral pH; spread environmental occurrence and the importance and reduced ferrous Fe (Fe(ii)), which is easily soluble of microbial Fe redox cycling for the degradation and and therefore more bioavailable. Fe speciation and bio‑ preservatio­n of C and the fate of many nutrients availability are dynamically controlled by the prevalent and contaminants9–11, we still lack a comprehensive changing redox conditions. Redox reactions of Fe with understanding of the mechanisms and pathways of C, N, O and S drive global biogeochemical cycles, as the electron transfer in Fe(ii)-oxidizing and Fe(iii)-reducing redox potential of the Fe(iii)–Fe(ii) redox couple lies bacteria. Unlike electron transfer between other major between the redox potentials of the major C, N, O or S inorganic redox species, electron transfer to and from species redox couples. Although microbial Fe oxidation Fe can be mediated by various cellular pathways. The had been described by the early nineteenth century1, the genes that are involved in gaining energy from oxidizing prevailing view in the early twentieth century was that Fe(ii) or reducing Fe(iii) are only known for a few bac‑ Fe cycling was mainly mediated abiotically by chemical teria, such as Rhodopseudomona­s palustris strain TIE‑1 – (REFS 12–14) reactions with molecular oxygen (O2), nitrite (NO2 ), and Shewanella oneidensis strain MR‑1 . Geomicrobiology, Center divalent and tetravalent manganese (Mn), various S spe‑ Gene families that encode proteins with a potential role for Applied Geosciences, University of Tübingen, cies and organic C. Since the discovery of neutrophilic in Fe(ii) oxidation or Fe(iii) reduction within different 2–5 Sigwartstrasse 10, 72076 Fe‑metabolizing bacteria , we have entered a ‘golden microbial taxa generally have low sequence identity, Tübingen, Germany. age’ of Fe geomicrobiology. All redox processes that were although some homologues of key genes have recently Correspondence to A.K. previously assumed to be purely abiotic (for example, been identified15–18. e‑mail: andreas.kappler@ oxidation of Fe(ii) by O or photochemical oxidation of The increased understanding of the genetic and uni‑tuebingen.de 2 doi:10.1038/nrmicro3347 Fe(ii)) are now known to also be microbially mediated. mechanistic pathways that are involved in Fe geomicro‑ Published online However, the contribution of microorganisms alone biology over the past 25 years has now converged with 20 October 2014 may not be sufficient to interpret the observed spatial the understanding of the abiotic chemical pathways NATURE REVIEWS | MICROBIOLOGY VOLUME 12 | DECEMBER 2014 | 797 © 2014 Macmillan Publishers Limited. All rights reserved REVIEWS Microbially mediated reactions Chemically mediated reactions – Microaerophiles O2 hν NO3 ROS 2+ + 4Fe + 10H2O + O2 → 4Fe(OH)3 + 8H Oxidation 2+ 3+ • – Fe + O2 → Fe + O2 Gallionella spp., Leptothrix spp., 2+ • – + 3+ Fe + O2 + 2H → Fe + H2O2 Mariprofundus spp., Sideroxydans spp. 2+ + 3+ • Fe + H2O2 + H → Fe + OH + H2O Fe(III) 2+ • + 3+ Aerobic Fe + OH + H → Fe + H2O Photoferrotrophs ROS hν Reduction – 2+ • – 2+ HCO3 + Fe + 10H2O → O • – O + Fe(III) → O + Fe + 2 O2 2 2 (CH2O) + 4Fe(OH)3 + 7H Rhodopseudomonas palustris TIE-1 hν Light reactions Rhodobacter sp. SW2 hν Photic Reduction Chlorobium ferrooxidans (KoFox) hν Thiodictyon sp. F4 hν Fe(III)–L → Fe(II)–L – Nitrogen species NO3 -reducing Fe(II)-oxidizers NO – NO 2+ – 3 x Oxidation 10Fe + 2NO3 + 24H2O → 4Fe2+ + 2NO – + 5H O → Reduction + Reduction Nitrate 2 2 10Fe(OH)3 + N2 + 18H + 4FeOOH + N2O + 6H + NH4 2+ – + Acidovorax spp., KS, 2002 Fe + NO2 + 2H → FeOOH + NO + H2O 2+ + 1 1 Thiobacillus denitrificans Fe + NO + H → FeOOH + /2 N2O + /2 H2O Oxidation Oxidation Fe-ammox Manganese MnO2 Manganese + + NH4 + 6FeOOH + 10H → Oxidation – 2+ 2+ NO2 + 6Fe + 10H2O 2Fe + MnO2 + 2H2O → Mn2+ + 2FeOOH + 2H+ Unknown HumS HumS Fe(III)-reducing organic C and/or organic C Iron H -oxidizers Reduction 2 – H Fe(III) + HumS HumS + Fe(II) – + 2 → 4FeOOH + CH3CHOHCOO + 7H → 2+ – – 4Fe + CH3COO + HCO3 + 6H2O Sulphur species 2Fe(OH) + H 2Fe2+ + 2H O H2S 2 → 2 Fe(II) Reduction Sulphur 0 Geobacter spp., Shewanella spp, 2FeOOH + 3H2S → 2FeS + S + 4H2O Albidoferax ferrireducens, Geothrix spp. Figure 1 | Microbially and chemically mediated reactions that form the biogeochemical Fe cycle. Microbially mediated iron (Fe) redox reactions are shown on the left-hand side and abiotic Fe redox transformationsNature Reviews are |shown Microbiology on the right-hand side, listed in a thermodynamic order (although some of these reactions may overlap in the natural environment). Within the oxic zone, microaerophilic Fe(ii) oxidizers oxidize ferrous Fe (Fe(ii)) using oxygen (O2). Reactive •− oxygen species (ROS) can oxidize Fe(ii), and superoxide (O2 ) can abiotically reduce ferric iron (Fe(iii)). Within the photic zone, phototrophic microorganisms oxidize Fe(ii) and photochemical reactions reduce Fe(iii) that is bound to organic – ligands (L). Mixotrophic and autotrophic nitrate (NO3 )-dependent Fe(ii) oxidation is restricted to anoxic conditions in the – denitrification zone. NO3 -reducing Fe(ii)-oxidizing bacteria use Fe(ii) as an electron donor. Fe–ammox bacteria couple + the oxidation of ammonium (NH4 ) to Fe(iii) reduction. Fe(ii) can be chemically oxidized via chemodenitrification by reactive nitrogen (N) species. Fe(ii) is abiotically oxidized by manganese (Mn) via surface-catalysed reactions. Fe(iii)-reducing microorganisms can reduce Fe(iii) coupled to the oxidation of various electron donors such as organic carbon (C) and H2. Electron-rich (that is, reduced) humic substances (HumS) abiotically reduce Fe(iii) to Fe(ii). Fe(iii) is – chemically reduced by hydrogen sulphide (H2S) to ferrous sulphide (FeS) species. The different gradients of O2, light, NO3 and Fe(ii) and Fe(iii) in a redox-stratified environmental system are shown, as well as where the different biotic and abiotic Fe redox transformations are expected to take place. that are involved in environmental Fe cycling. So far, Microbially mediated Fe(ii) oxidation by O2. many studies have focused on either abiotic or biotic Microaerophilic­ Fe(ii) oxidizers are lithotrophic bacteria processes; however, these processes are interconnected that oxidize Fe(ii) with O2 according to the following and cannot be studied separately if we are to truly stoichiometric equation5 (FIG. 1): Microaerophilic A term used to describe understand environmental biogeochemical Fe cycling. 2+ + 4Fe + 10H2O + O2 → 4Fe(OH)3 + 8H (1) microbial metabolism that Therefore, a current challenge is to discern abiotic from requires oxygen (O2) microbially mediated Fe redox processes and to esti‑ Phylogenetically, these bacteria belong to the phy‑ concentrations to be very low; mate their overall contributions to the Fe biogeochemi‑ lum Proteobacteria, which includes the freshwater gen‑ for example, microaerophilic 19 20 21 ferrous iron Fe(ii)-oxidizing cal cycle. In this Review, we discuss the most important era Leptothrix , Gallionella and Sideroxydans and the microbially mediated and abiotic reactions and address marine genus Mariprofundus22. Microaerophilic Fe(ii) bacteria function when the O2 concentration is below 50 μM. their interactions within the biogeochemical Fe cycle. oxidizers are common in many freshwater and marine (REFS 5,23,24) environments that are exposed to O2 , and Lithotrophic Fe(ii) oxidation by O their growth is severely retarded under anoxic conditions, A term used to describe 2 NO –) microbial metabolism that uses The high redox potential of O2 and its one-electron with the exception of the nitrate ( 3 -reducing Fe(ii)- 25 inorganic substrates as transfer derivatives readily initiates the exergonic abiotic oxidizing co‑culture KS that contains a Sideroxydans
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