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Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms

Abstract

Electroactive microorganisms markedly affect many environments in which they establish outer-surface electrical contacts with other cells and minerals or reduce soluble extracellular redox-active molecules such as flavins and humic substances. A growing body of research emphasizes their broad phylogenetic diversity and shows that these microorganisms have key roles in multiple biogeochemical cycles, as well as the microbiome of the gut, anaerobic waste digesters and metal corrosion. Diverse bacteria and archaea have independently evolved cytochrome-based strategies for electron exchange between the outer cell surface and the cell interior, but cytochrome-free mechanisms are also prevalent. Electrically conductive protein filaments, soluble electron shuttles and non-biological conductive materials can substantially extend the electronic reach of microorganisms beyond the surface of the cell. The growing appreciation of the diversity of electroactive microorganisms and their unique electronic capabilities is leading to a broad range of applications.

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Fig. 1: Phylogenetic diversity of electroactive microorganisms.
Fig. 2: Functional roles of electroactive microorganisms.
Fig. 3: Mechanisms for electron transport across the outer surface.
Fig. 4: Mechanisms to enhance extracellular electron transport to solid-phase electron acceptors and long-range electron transport.
Fig. 5: Applications emerging from the study of electroactive microorganisms.

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Acknowledgements

The authors thank their former laboratory colleagues at the US Geological Survey and the University of Massachusetts, as well as collaborators too numerous to list, who have contributed to the study of electroactive microorganisms for more than 35 years. They apologize to all investigators whose excellent work could not be cited due to space constraints.

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D.E.H. performed the phylogenetic analysis displayed in Fig. 1. D.R.L. reviewed the literature and assembled additional figures. Both authors edited and approved the final text.

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Correspondence to Derek R. Lovley.

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Glossary

Microbial electrochemical technologies

Applications that rely on microorganism–electrode electron exchange, such as microbial fuel cells.

Electroactive microorganisms

Microorganisms that can exchange electrons with their extracellular environment.

Electromicrobiomes

Environments in which microorganisms electrically interact with each other and/or their extracellular environment.

Extracellular electron transfer

(EET). Electron transfer to or from another cell, electron acceptors not in solution or dissolved compounds that do not enter the cell.

Electrogens

Microorganisms that generate electricity in a bioelectrochemical system or donate electrons to natural extracellular electron acceptors.

Electrotrophs

Microorganisms that consume electricity in a bioelectrochemical system or accept electrons from natural extracellular electron donors.

Fe(III) oxides

Collectively, the diverse, poorly soluble Fe(III) minerals of various degrees of crystallinity that are abundant in most soils and sediments.

Anammox bacteria

Bacteria that combine ammonium with nitrite or nitrate to form nitrogen gas.

Cable bacteria

Bacteria that form filaments comprising thousands of cells to conduct electrons from anaerobic to aerobic zones of soils and sediments.

Direct interspecies electron transfer

(DIET). Electron exchange between two microbial species via electrical connections rather than a diffusible electron carrier such as H2.

Electron shuttles

Redox active molecules that can be reversibly oxidized and reduced that, at catalytic quantities, serve as an intermediary for extracellular electron transfer between cells and extracellular electron acceptors or donors.

Chelators

In the context of electromicrobiology, an organic compound that tightly binds and solubilizes metal ions, notably Fe(III).

Pilin

A monomer protein that bacteria assemble into pili.

Biofilms

A collective of one or more species of microorganisms adhered to a surface.

Archaella

Filaments produced by archaea for motility or attachment, which in some instances may be electrically conductive.

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Lovley, D.R., Holmes, D.E. Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms. Nat Rev Microbiol (2021). https://doi.org/10.1038/s41579-021-00597-6

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