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  • Review Article
  • Published:

The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle

Nature Reviews Microbiology volume 12, pages 797–808 (2014)Cite this article

Subjects

Key Points

  • Biogeochemical iron (Fe) cycling in pH-circumneutral environments involves concurrent microbially and chemically driven ferrous iron (Fe(II)) oxidation and Fe(III) reduction processes, which must be distinguished in the field and in the laboratory with carefully designed control experiments.

  • Microbial Fe(II) oxidation can be coupled to reduction of molecular oxygen (O2) by microaerophilic Fe(II) oxidizers, to nitrate (NO3−) reduction by NO3−-reducing Fe(II) oxidizers and to light energy by anoxygenic photosynthetic Fe(II) oxidizers. Whereas the microaerophiles and NO3− reducers need to overcome competition from abiotic Fe reactions with O2 and NO2−, the photoferrotrophs can benefit from photochemical Fe reduction that produces Fe(II).

  • At circumneutral pH and high O2 concentrations, chemical Fe(II) oxidation with O2 is kinetically very fast, whereas neutrophilic Fe(II)-oxidizing microorganisms exploit slower kinetics under micro-oxic conditions. Although a kinetic expression that includes chemical and microbial Fe(II) oxidation has not yet been formulated and continues to be a challenge, both reactions can be expressed individually and must account for both homogeneous and heterogenous Fe(II) oxidation.

  • Dissimilatory reduction of Fe(III) oxides and oxyhydroxides is a challenge for microorganisms as their cell envelopes are impermeable to poorly soluble Fe(III) minerals. In order to overcome this limitation, environmental Fe(III)-reducing microorganisms have developed electron-transfer strategies including the use of multihaem c-type cytochromes for direct electron transfer, electron shuttling via native and environmental extracellular electron shuttles, Fe(III) dissolution by chelating agents and electron transfer via conductive pili.

  • One-electron transfers between Fe and reactive oxygen species (ROS) drive Fe redox transformations in sunlit natural waters, enhanced by photochemical production of ROS in waters containing organic carbon and O2. Recent reports of biological ROS production by diverse microorganisms pushes the importance of ROS-driven Fe cycling into darker waters.

  • Many Fe(II)-oxidizing and Fe(III)-reducing bacteria are metabolically flexible, which helps them to adapt to environmental fluctuations of electron donors and acceptors; they actively construct niches to cope with competition from other microorganisms and to overcome substrate limitation by competing chemical reactions.

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.

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Figure 1: Microbially and chemically mediated reactions that form the biogeochemical Fe cycle.
Figure 2: Microbially and chemically mediated Fe(II) oxidation by O2.
Figure 3: Mechanisms of electron transfer from microorganisms to Fe(III) minerals.
Figure 4: Designing the proper controls and recognizing pitfalls during acidification for Fe-extraction procedures.

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Acknowledgements

The authors acknowledge funding for several research grants from the German research Foundation (DFG), a Marie Curie ERG grant to C.S. (PERF04-GA-2008-239252), a Margarete von Wrangell grant to C.S. and a Landesgraduiertenfoerderung fellowship to E.D.M. (GZ l 1.2_7631.2/Melton). This study was also supported by the European Research Council under the European Union' s Seventh Framework Program (FP/2007–2013)/ERC Grant, agreement number 307320 — MICROFOX.

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  1. Geomicrobiology, Center for Applied Geosciences, University of Tübingen, Sigwartstrasse 10, 72076, Tübingen, Germany

    Emily D. Melton, Elizabeth D. Swanner, Sebastian Behrens, Caroline Schmidt & Andreas Kappler

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Glossary

Fe speciation

Refers to the redox state of iron (Fe) and the identity of its ligands. The two most common environmental Fe redox species are Fe(II) and Fe(III).

Microaerophilic

A term used to describe microbial metabolism that requires oxygen (O2) concentrations to be very low; for example, microaerophilic ferrous iron Fe(II)-oxidizing bacteria function when the O2 concentration is below 50 μM.

Lithotrophic

A term used to describe microbial metabolism that uses inorganic substrates as electron donors.

Redoxclines

The interfaces between two spatially distinct areas that differ in chemical composition and redox potential; they are usually used to describe a transition from oxic to anoxic conditions.

c-type cytochromes

Small haem-containing proteins that have an important role in respiratory electron transfer reactions.

Reactive oxygen species

(ROS). Oxygen-containing species that have unpaired electrons, making them highly reactive towards transition metals such as iron and copper.

Heterogeneous Fe(II) oxidation

Oxidation of ferrous iron (Fe(II)), where dissolved Fe(II) is adsorbed to a mineral surface, which functions as a catalyst, and the oxidant is in a different physical phase; for example, dissolved oxygen.

Homogeneous Fe(II) oxidation

A chemical reaction in which both ferrous iron (Fe(II)) and the oxidant are in the same physical phase; for example, dissolved.

Two-line ferrihydrite

A nano-scale ferric iron (Fe(III)) oxyhydroxide mineral with an average primary crystallite size of 2–3 nm and a formula of Fe10O14(OH)2. Two-line refers to the two diffraction signals observed by X-ray diffraction.

Lepidocrocite

An orange-coloured FeOOH polymorph (γ-FeOOH); it is a ferric iron oxyhydroxide mineral.

Akaganeite

A FeOOH polymorph (β-FeOOH); it is a ferric iron oxyhydroxide mineral that is yellowish-brown in color and typically occurs in saline environments.

Goethite

An FeOOH polymorph (α-FeOOH); it is a ferric iron oxyhydroxide mineral. It is yellow to dark brown depending on the crystal size.

Colloids

Particles that are dispersed in a liquid or gas within a size fraction ranging from 1 nm to 1 μm in diameter.

Siderophores

Microbially produced organic molecules that are excreted in order to complex ferric iron (Fe(III)) ions, so the Fe can be taken up into the cells in a dissolved phase.

Comproportionation

A chemical reaction in which two reactants of the same element with a different oxidation state react to create a product with a single oxidation state.

Disproportionation

A chemical reaction in which a reactant is split into two species of the same chemical element with different oxidation states: one more oxidized and the other more reduced.

Mixotrophic

A term used to describe microbial metabolism that uses an organic substrate as a carbon source and an inorganic compound as electron donor.

Heterogeneous surface catalysis

A reaction in which the catalyst that facilitates the reaction of liquids or gases is present in the solid state.

Humic substances

(HumS). Organic molecules that are present in terrestrial and aquatic environments with a wide variety of structures that result from the degradation and polymerization of biopolymers, such as lignin, lipids, proteins, and polysaccharides. Diverse functional groups within the humic substance molecules are redox-active and have electron-donating or -accepting capacities.

Humic and fulvic acids

Humic acids are humic substances that are insoluble at low pH values, partially soluble at neutral pH and completely soluble at alkaline pH. Fulvic acids are humic substances that are soluble at all pH values.

First order kinetics

A term used to describe the kinetics of a reaction in which the concentration of one of the reactants is linearly related to the reaction rate.

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Melton, E., Swanner, E., Behrens, S. et al. The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol 12, 797–808 (2014). https://doi.org/10.1038/nrmicro3347

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