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 pr...

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Published in:	Nature reviews. Microbiology Vol. 14; no. 10; pp. 651 - 662
Main Authors:	Shi, Liang, Dong, Hailiang, Reguera, Gemma, Beyenal, Haluk, Lu, Anhuai, Liu, Juan, Yu, Han-Qing, Fredrickson, James K.
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 01-10-2016 Nature Publishing Group
Subjects:	631/326/171 631/326/2522 631/326/41/1969 631/326/41/2537 631/326/41/88 631/326/47 Archaea - metabolism Bacteria - genetics Bacteria - metabolism BASIC BIOLOGICAL SCIENCES Biodegradation, Environmental Biofuels Bioremediation Biotechnology Biotechnology - methods Carbon dioxide Cell interactions Cytochromes c - genetics Electron Transport Electrons Energy resources Infectious Diseases Life Sciences Medical Microbiology Metabolic Networks and Pathways - genetics Metabolism Microbiological research Microbiology Microorganisms Mineral metabolism Minerals Minerals - chemistry Minerals - metabolism Nanotechnology Nanowires Nitrates Observations Oxidation Oxidation-Reduction Parasitology Proteins Respiration review-article Virology China
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Abstract	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. Microorganisms with electron transfer capabilities, such as metal-reducing microorganisms, use specialized systems to exchange electrons between minerals and cells. In this Review, Shi et al . summarize the underlying molecular mechanisms, such as cytochromes and nanowires, and biotechnological applications. 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.
AbstractList	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. 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. Microorganisms with electron transfer capabilities, such as metal-reducing microorganisms, use specialized systems to exchange electrons between minerals and cells. In this Review, Shi et al . summarize the underlying molecular mechanisms, such as cytochromes and nanowires, and biotechnological applications. 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.
Audience	Academic
Author	Shi, Liang Dong, Hailiang Beyenal, Haluk Liu, Juan Yu, Han-Qing Lu, Anhuai Fredrickson, James K. Reguera, Gemma
Author_xml	– sequence: 1 givenname: Liang surname: Shi fullname: Shi, Liang email: liang.shi@cug.edu.cn organization: Department of Biological Sciences and Technology, School of Environmental Studies, China University of Geoscience in Wuhan – sequence: 2 givenname: Hailiang surname: Dong fullname: Dong, Hailiang email: dongh@miamioh.edu organization: Department of Geology and Environmental Earth Science, Miami University, State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences – sequence: 3 givenname: Gemma surname: Reguera fullname: Reguera, Gemma organization: Department of Microbiology and Molecular Genetics, Michigan State University – sequence: 4 givenname: Haluk surname: Beyenal fullname: Beyenal, Haluk organization: The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University – sequence: 5 givenname: Anhuai surname: Lu fullname: Lu, Anhuai organization: School of Space and Earth Sciences, Peking University – sequence: 6 givenname: Juan surname: Liu fullname: Liu, Juan organization: College of Environmental Sciences and Engineering, Peking University – sequence: 7 givenname: Han-Qing surname: Yu fullname: Yu, Han-Qing organization: Department of Chemistry, University of Science and Technology of China – sequence: 8 givenname: James K. surname: Fredrickson fullname: Fredrickson, James K. organization: Biological Sciences Division, Pacific Northwest National Laboratory
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Snippet	Key Points Specific microorganisms use metal-containing minerals as electron sinks for heterotrophy-based respiration and electron and/or energy sources for... Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is...
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SubjectTerms	631/326/171 631/326/2522 631/326/41/1969 631/326/41/2537 631/326/41/88 631/326/47 Archaea - metabolism Bacteria - genetics Bacteria - metabolism BASIC BIOLOGICAL SCIENCES Biodegradation, Environmental Biofuels Bioremediation Biotechnology Biotechnology - methods Carbon dioxide Cell interactions Cytochromes c - genetics Electron Transport Electrons Energy resources Infectious Diseases Life Sciences Medical Microbiology Metabolic Networks and Pathways - genetics Metabolism Microbiological research Microbiology Microorganisms Mineral metabolism Minerals Minerals - chemistry Minerals - metabolism Nanotechnology Nanowires Nitrates Observations Oxidation Oxidation-Reduction Parasitology Proteins Respiration review-article Virology
Title	Extracellular electron transfer mechanisms between microorganisms and minerals
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