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Extracellular electron transfer mechanisms between microorganisms and minerals

Key Points

  • Specific microorganisms use metal-containing minerals as electron sinks for heterotrophy-based respiration and electron and/or energy sources for autotrophic growth.

  • The microbial cell envelope is an electrical and physical barrier that can be overcome by pathways that consist of redox proteins (for example, c-type cytochromes) and structural proteins, which span the entire width of the microbial cell envelope and enable the exchange of electrons with extracellular minerals.

  • Some microorganisms can extend their redox-active surface beyond the confines of the cell envelope by forming microbial nanowires, which transfer electrons to distal minerals.

  • c-Type cytochromes, microbial nanowires and other cellular structures are, or are suggested to be, involved in intercellular electron transfer between the same or different species or even domains.

  • Minerals that contain metal ions can also function as electrical conductors and batteries to facilitate electron exchange among different groups of microorganisms.

  • Microorganisms with extracellular electron transfer capabilities have been harnessed for the bioremediation of environmental contaminants, the production of biofuels, the production of nanomaterials with novel properties and biomining of copper, gold and other metals.

Abstract

Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is neither physically permeable to minerals nor electrically conductive, microorganisms have evolved strategies to exchange electrons with extracellular minerals. In this Review, we discuss the molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species. Microorganisms that have extracellular electron transfer capability can be used for biotechnological applications, including bioremediation, biomining and the production of biofuels and nanomaterials.

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Figure 1: Electrical interplay between microorganisms and minerals.
Figure 2: The proposed Mtr, Pcc, Pio and Mto extracellular electron transfer pathways.
Figure 3: The proposed microbial structures for intercellular electron transfer.

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Acknowledgements

The authors acknowledge research grant funding from the Office of Biological and Environmental Research/Subsurface Biogeochemical Research Program of the US Department of Energy (L.S., H.D., G.R., H.B. and J.K.F.), the US National Science Foundation (H.D., G.R. and H.B.), the US National Institutes of Health and National Institute of Environmental Health Sciences (L.S. and G.R.), the US Office of Naval Research (H.B.), the National Natural Science Foundation of China (H.D., A.L., J.L. and H.Q.Y.), the 973 program of China (A.L.) and the One-Hundred Talented Researchers Project of the Chinese Academy of Science (H.Q.Y.). The authors also thank D. Lovley, J. Gralnick and an anonymous reviewer for their constructive comments.

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Glossary

Autotrophic growth

A metabolic process that supports microbial growth and uses light or chemical energy to fix CO2 for the synthesis of organic matter.

Respiratory terminal electron acceptors

A group of oxidizing agents, such as O2, NO3 and Fe(III), that receive the electrons that are released from the metabolic oxidation of organic and inorganic substrates by microorganisms.

Dissimilatory metal-reducing microorganisms

These microorganisms carry out a biochemical reaction during which metal ions are reduced but not incorporated into the cells.

Semiconductive minerals

Minerals the conductivity of which is between that of insulators and that of most metals.

S-Layer

A cell envelope structure that consists of proteins or glycoproteins and is on the cell surface.

Quinone and quinol

A group of aromatic compounds that act as mobile components of the electron transport chain in the cytoplasmic membrane and can receive and donate electrons (quinone is the oxidized form and quinol the reduced form).

Photoreaction centre

A pigment–protein complex in the inner cytoplasmic membrane of photosynthetic bacterial cells, where it converts solar energy to chemical energy to support bacterial growth.

Multistep hopping mechanism

A redox conduction process in which electrons transfer sequentially from one charge-localizing redox centre (for example, the haem iron) to an adjacent one, such as along the haem chain of multihaem c-type cytochromes (c-Cyts).

Flavins

A group of organic compounds with a tricyclic aromatic moiety that can exist in three different redox states: oxidized (0 electron), semiquinone (1 electron) and reduced (2 electrons).

Bacterial type IVa pilins

Pilins that have the following characteristics: a leader peptide of 5–6 amino acids, an average polypeptide of 150 amino acids, an N-methylated amino-terminal residue of phenylalanine and an average disulfide-bonded region (D-region) of 22 amino acids.

Metallic-like electron transfer

A conduction process in which electrons are delocalized and can move freely without thermal activation, as in metals and conductive polymers.

Anodes

An electrode that accepts electrons.

Cathodes

An electrode that donates electrons.

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Shi, L., Dong, H., Reguera, G. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14, 651–662 (2016). https://doi.org/10.1038/nrmicro.2016.93

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