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An evolving view on biogeochemical cycling of iron

Abstract

Biogeochemical cycling of iron is crucial to many environmental processes, such as ocean productivity, carbon storage, greenhouse gas emissions and the fate of nutrients, toxic metals and metalloids. Knowledge of the underlying processes involved in iron cycling has accelerated in recent years along with appreciation of the complex network of biotic and abiotic reactions dictating the speciation, mobility and reactivity of iron in the environment. Recent studies have provided insights into novel processes in the biogeochemical iron cycle such as microbial ammonium oxidation and methane oxidation coupled to Fe(iii) reduction. They have also revealed that processes in the biogeochemical iron cycle spatially overlap and may compete with each other, and that oxidation and reduction of iron occur cyclically or simultaneously in many environments. This Review discusses these advances with particular focus on their environmental consequences, including the formation of greenhouse gases and the fate of nutrients and contaminants.

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Fig. 1: The biogeochemical iron cycle.
Fig. 2: Redox potentials of diverse Fe(ii)–Fe(iii) redox couples.
Fig. 3: Electron transfer mechanisms from microorganisms to Fe(iii) minerals.
Fig. 4: Overview of processes that can overlap and lead to cryptic iron cycling.

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Acknowledgements

The authors acknowledge funding for several research grants from the German Research Foundation (DFG), in particular the Collaborative Research Center CAMPOS (DFG grant agreement SFB 1253/1) and the priority programme EarthShape.

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A.K. and C.B. initiated the manuscript, designed the content, wrote the manuscript, created some of the figures, and compiled and revised all content. E.D.S., M.M., U.L. and J.M.B. wrote the manuscript and created some of the figures.

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Correspondence to Andreas Kappler.

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Nature Reviews Microbiology thanks J. Gralnick, who co-reviewed with A. Jain, J. Senko and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Glossary

Microaerophilic

Microorganisms that oxidize Fe(ii) at O2 concentrations in the tens of micromoles per litre range are microaerophilic Fe(ii) oxidizers.

Speciation

Describes the oxidation state and the identity of the coordinating ligands (for example, organic matter, chloride or sulfide).

Redox potentials

Redox potential (in millivolts) indicates the thermodynamic driving force for reduction or oxidation, for example, of an Fe(iii)–Fe(ii) pair.

Ferrihydrite

A poorly crystalline (short-range-ordered) iron(iii) oxyhydroxide mineral with a primary particle diameter in the low nanometre range (less than 6 nm), and a resulting large surface area and high reactivity.

Natural organic matter

(NOM). Mixture of organic compounds resulting in nature from the degradation of biopolymers (proteins, lipids, lignin, polysaccharides and so on) stemming from plants, microorganisms and animals.

Nanoparticles

Particles smaller than 100 nm in at least one dimension.

Colloids

Particles smaller than 1,000 nm in at least one dimension that are dispersed in a substance of another physical state (for example, mineral particles in a liquid).

Particulates

Particles larger than 1,000 nm in all dimensions.

Transmission electron microscopy

(TEM). An imaging technique using a beam of electrons transmitted through a thin specimen to obtain an image of the specimen down to atomic resolution, applied in physical, chemical and biological sciences. Can be used, for example, to characterize nanoparticles formed by iron-metabolizing microorganisms.

Scanning electron microscopy

(SEM). An imaging technique using a beam of electrons to scan the surface of a specimen to obtain information about the morphology, topography and surface structure. Applied, for example, to characterize cell–mineral structures of iron-metabolizing microorganisms.

Homogeneous Fe(ii) oxidation

The oxidation of reduced iron (Fe(ii)) by an oxidant that is in the same physical state (for example, oxidation of dissolved Fe2+ by dissolved O2).

Reactive oxygen species

(ROS). Very reactive compounds with unpaired electrons formed from molecular O2.

Lepidocrocite

A ferric iron oxyhydroxide polymorph (γ-FeOOH) with a yellow to reddish brown colour.

Goethite

A ferric iron oxyhydroxide polymorph (α-FeOOH) known for its use as a paint pigment and named after the poet Johann Wolfgang von Goethe.

Akageneite

A chloride-containing ferric iron oxyhydroxide polymorph (β-FeOOH) that typically forms in marine environments.

Heterogeneous Fe(ii) oxidation

The oxidation of iron (Fe(ii)) by an oxidant that is in a different physical state (for example, oxidation of sorbed Fe(ii) by dissolved O2).

Voltammetric microelectrodes

Electrodes with tip diameters in the micrometre range (the potential at the working electrode is varied and the resulting current is recorded). Such electrodes can be used to identify and quantify iron redox species with high spatial resolution (for example, in sediments).

c-type cytochrome

A protein that contains haem as a prosthetic group and is involved in oxidation and reduction reactions inside and outside the microbial cell.

Extracellular polymeric substances

Organic molecules consisting of polysaccharides and proteins, but also DNA and lipids, purposefully released by microorganisms into the environment (for example, during biofilm formation).

Humic substances

Stable organic molecules that are redox active and thought to form by humification; that is, the transformation of biomolecules (including lignin, proteins and polysaccharides). This formation theory has been questioned and is being gradually replaced by a soil continuum model.

Siderophores

Organic compounds produced and released by microorganisms in order to make otherwise poorly soluble Fe(iii) ions bioavailable for the cells and to facilitate their uptake.

Chemolithoautotrophic

Describes microorganisms that use energy from a chemical reaction of inorganic compounds (for example, oxidation of Fe(ii)) to fix carbon from CO2 into biomass.

Mixotrophs

Microorganisms using an inorganic electron source (for example Fe(ii)) in addition to an organic compound for their metabolism are termed mixotrophs, i.e. mixotrophic microorganisms.

Fe(iii) reducers

Microorganisms that specialize in gaining energy by coupling Fe(iii) reduction with the oxidation of an electron donor (for example, an organic compound).

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Kappler, A., Bryce, C., Mansor, M. et al. An evolving view on biogeochemical cycling of iron. Nat Rev Microbiol 19, 360–374 (2021). https://doi.org/10.1038/s41579-020-00502-7

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