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Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction

Abstract

Iron (Fe) has long been a recognized physiological requirement for life, yet for many microorganisms that persist in water, soils and sediments, its role extends well beyond that of a nutritional necessity. Fe(II) can function as an electron source for iron-oxidizing microorganisms under both oxic and anoxic conditions and Fe(III) can function as a terminal electron acceptor under anoxic conditions for iron-reducing microorganisms. Given that iron is the fourth most abundant element in the Earth's crust, iron redox reactions have the potential to support substantial microbial populations in soil and sedimentary environments. As such, biological iron apportionment has been described as one of the most ancient forms of microbial metabolism on Earth, and as a conceivable extraterrestrial metabolism on other iron-mineral-rich planets such as Mars. Furthermore, the metabolic versatility of the microorganisms involved in these reactions has resulted in the development of biotechnological applications to remediate contaminated environments and harvest energy.

Key Points

  • The recent identification of anaerobic microbial Fe(II) oxidation closed a gap in the iron redox cycle. Together with microbial Fe(III) reduction, these metabolisms are now known to transcend phylogenetic boundaries and have been shown to contribute significantly to soil and sediment biogeochemistry and mineralogy in anaerobic environments.

  • It is now accepted that microorganisms primarily control iron redox chemistry in most environments. Under anoxic conditions, Fe(III) oxide minerals are reduced by Fe(III)-reducing microorganisms (FRM). The ubiquity of FRM and their phylogenetic diversity makes this microbial metabolism globally significant. FRM can use both organic (CO2) and inorganic (H2) electron donors. The microbially mediated reduction of Fe(III) oxide minerals can generate both aqueous and solid-phase Fe(II)-bearing minerals such as siderite.

  • Microbially mediated Fe(II) oxidation is carried out by Fe(II)-oxidizing microorganisms (FOM). FOM are ubiquitous and have been identified in many different environments. The aerobic microbial oxidation of Fe(II) has been known for more than 100 years, but anaerobic Fe(II) oxidation by FOM was only identified in the early 1990s. Anaerobic Fe(II) oxidation by FOM can occur in both the presence and absence of light. FOM can couple Fe(II) oxidation to the reduction of nitrate, perchlorate and chlorate. Nitrate-dependent FOM can oxidize solid-phase Fe(II), including Fe(II) associated with structural Fe in minerals such as almandine and staurolite. Biogenic Fe(II) oxide minerals include magnetite and hematite, and nitrate-dependent Fe(II) oxidation has been implicated as having a direct role in the formation of banded iron formations in Precambrian Earth.

  • Recent evidence indicates that both of these metabolic processes have direct bioremediative and biotechnological applications. Anaerobic oxidation of Fe(II) by FOM can lead to the precipitation of biogenic Fe(III) oxides such as goethite and hematite. This provides a mechanism for the immobilization of heavy metals and metalloids through co-precipitation or physical envelopment. The anaerobic formation of biogenic Fe(III)-oxide-containing minerals has therefore been identified as a plausible bioremediation strategy for heavy metals and radionuclides. In addition to the ability to utilize insoluble Fe(III) as an electron acceptor, FRM such as Geobacter spp. can alternatively pass electrons onto the surface of an electrode (anode). This has led to the development of microbial fuel cells for the generation of electricity. FRM can also transform various organic contaminants (including benzene, toluene and phenol) and heavy metal and radionuclide contaminants (including uranium) and so might also be useful in bioremediation.

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Acknowledgements

Research on microbial redox cycling of iron in the laboratories of J.D.C. and L.A.A. is supported by grants from the US Department of Energy Environmental Remediation Sciences Program.

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Correspondence to John D. Coates.

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Glossary

Lithotrophic

A lithotrophic organism uses an inorganic substrate (usually of mineral origin) to obtain energy for growth.

Heterotrophic

A heterotrophic organism requires organic compounds as a carbon source.

Suboxic

An environment with a partial pressure of oxygen that is substantially lower than the atmospheric oxygen content.

Anoxic

An environment lacking oxygen.

Neoteric environments

Modern environments.

Electron sink

A compound that receives electrons as an endpoint of an oxidative reaction.

Bioturbation

The disturbance of sediment layers by biological activity.

Microaerophilic

An organism that is an obligate anaerobe but can survive in environments where the partial pressure of oxygen is substantially lower than in the atmosphere.

Phototrophic

A phototrophic organism obtains energy for growth from sunlight; carbon is derived from inorganic carbon (carbon dioxide) or organic carbon.

Neutrophilic Fe(II) oxidation

Microbial Fe(II) oxidation that occurs at circumneutral pH values (pH 7).

Psychrophilic

An organism that grows optimally in a cold environment (<15°C).

Mesophilic

An organism that grows optimally in a moderate environment (25–45°C).

Hyperthermophilic

An organism that grows optimally in hot environments (>80°C).

Autotrophic

An autotrophic organism uses inorganic carbon (carbon dioxide) as a carbon source.

Chemolithoautotrophic

An organism that obtains energy from inorganic compounds and carbon from carbon dioxide.

Mixotrophy

A mixotrophic organism uses an inorganic chemical energy source and organic compounds as a carbon source.

Eutrophic

Eutrophic waters are rich in minerals and organic nutrients.

Oligotrophic environment

An environment that is relatively low in nutrients and cannot support much plant life.

Thermophilic

An organism that grows optimally at temperatures ranging from 45–80°C.

Acidophilic

An organism that grows in an acid environment (<pH 6).

Alkaliphilic

An organism that grows in an alkaline environment (pH 9–pH 11).

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Figure 1: The microbially mediated iron redox cycle.
Figure 2: Potential electron donors and acceptors: a redox tower.
Figure 3: Phylogenetic affiliation of microorganisms contributing to iron redox cycling.
Figure 4: Microbial strategies mediating electron transfer to insoluble Fe(III) oxides.
Figure 5: Physiological model of the biochemistry involved in microbial Fe(III) reduction by Shewanella and Geobacter spp.