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Geomicrobiology

A Hybrid Extracellular Electron Transfer Pathway Enhances the Survival of Vibrio natriegens

Bridget E. Conley, Matthew T. Weinstock, Daniel R. Bond, Jeffrey A. Gralnick
Robert M. Kelly, Editor
Bridget E. Conley
aBioTechnology Institute and Department of Plant and Microbial Biology, University of Minnesota—Twin Cities, St. Paul, Minnesota, USA
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Matthew T. Weinstock
bAbSci LLC, Vancouver, Washington, USA
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Daniel R. Bond
aBioTechnology Institute and Department of Plant and Microbial Biology, University of Minnesota—Twin Cities, St. Paul, Minnesota, USA
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Jeffrey A. Gralnick
aBioTechnology Institute and Department of Plant and Microbial Biology, University of Minnesota—Twin Cities, St. Paul, Minnesota, USA
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Robert M. Kelly
North Carolina State University
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DOI: 10.1128/AEM.01253-20
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ABSTRACT

Vibrio natriegens is the fastest-growing microorganism discovered to date, making it a useful model for biotechnology and basic research. While it is recognized for its rapid aerobic metabolism, less is known about anaerobic adaptations in V. natriegens or how the organism survives when oxygen is limited. Here, we describe and characterize extracellular electron transfer (EET) in V. natriegens, a metabolism that requires movement of electrons across protective cellular barriers to reach the extracellular space. V. natriegens performs extracellular electron transfer under fermentative conditions with gluconate, glucosamine, and pyruvate. We characterized a pathway in V. natriegens that requires CymA, PdsA, and MtrCAB for Fe(III) citrate and Fe(III) oxide reduction, which represents a hybrid of strategies previously discovered in Shewanella and Aeromonas. Expression of these V. natriegens genes functionally complemented Shewanella oneidensis mutants. Phylogenetic analysis of the inner membrane quinol dehydrogenases CymA and NapC in gammaproteobacteria suggests that CymA from Shewanella diverged from Vibrionaceae CymA and NapC. Analysis of sequenced Vibrionaceae revealed that the genetic potential to perform EET is conserved in some members of the Harveyi and Vulnificus clades but is more variable in other clades. We provide evidence that EET enhances anaerobic survival of V. natriegens, which may be the primary physiological function for EET in Vibrionaceae.

IMPORTANCE Bacteria from the genus Vibrio occupy a variety of marine and brackish niches with fluctuating nutrient and energy sources. When oxygen is limited, fermentation or alternative respiration pathways must be used to conserve energy. In sedimentary environments, insoluble oxide minerals (primarily iron and manganese) are able to serve as electron acceptors for anaerobic respiration by microorganisms capable of extracellular electron transfer, a metabolism that enables the use of these insoluble substrates. Here, we identify the mechanism for extracellular electron transfer in Vibrio natriegens, which uses a combination of strategies previously identified in Shewanella and Aeromonas. We show that extracellular electron transfer enhanced survival of V. natriegens under fermentative conditions, which may be a generalized strategy among Vibrio spp. predicted to have this metabolism.

FOOTNOTES

    • Received 26 May 2020.
    • Accepted 28 July 2020.
    • Accepted manuscript posted online 31 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

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A Hybrid Extracellular Electron Transfer Pathway Enhances the Survival of Vibrio natriegens
Bridget E. Conley, Matthew T. Weinstock, Daniel R. Bond, Jeffrey A. Gralnick
Applied and Environmental Microbiology Sep 2020, 86 (19) e01253-20; DOI: 10.1128/AEM.01253-20

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A Hybrid Extracellular Electron Transfer Pathway Enhances the Survival of Vibrio natriegens
Bridget E. Conley, Matthew T. Weinstock, Daniel R. Bond, Jeffrey A. Gralnick
Applied and Environmental Microbiology Sep 2020, 86 (19) e01253-20; DOI: 10.1128/AEM.01253-20
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KEYWORDS

anaerobic respiration
metal reduction
survival

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