1. Biochemistry and Chemical Biology
  2. Microbiology and Infectious Disease
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An elusive electron shuttle from a facultative anaerobe

  1. Emily Mevers
  2. Lin Su
  3. Gleb Pishchany
  4. Moshe Baruch
  5. Jose Cornejo
  6. Elissa Hobert
  7. Eric Dimise  Is a corresponding author
  8. Caroline M Ajo-Franklin
  9. Jon Clardy  Is a corresponding author
  1. Harvard Medical School, United States
  2. Lawrence Berkeley National Laboratory, University of California, Berkeley, United States
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Cite this article as: eLife 2019;8:e48054 doi: 10.7554/eLife.48054

Abstract

Some anaerobic bacteria use insoluble minerals as terminal electron acceptors and discovering the ways in which electrons move through the membrane barrier to the exterior acceptor forms an active field of research with implications for both bacterial physiology and bioenergy. A previous study suggested that Shewanella oneidensis MR-1 utilizes a small, polar, redox active molecule that serves as an electron shuttle between the bacteria and insoluble acceptors, but the shuttle itself has never been identified. Through isolation and synthesis, we identify it as ACNQ (2-amino-3-carboxy-1,4-naphthoquinone), a soluble analog of menaquinone. ACNQ is derived from DHNA (1,4-dihydroxy-2-naphthoic acid) in a non-enzymatic process that frustrated genetic approaches to identify the shuttle. Both ACNQ and DHNA restore reduction of AQDS under anaerobic growth in menaquinone-deficient mutants. Bioelectrochemistry analyses reveal that ACNQ (-0.32 VAg/AgCl) contributes to the extracellular electron transfer (EET) as an electron shuttle, without altering menaquinone generation or EET related cytochrome c expression.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Emily Mevers

    Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7986-5610

  2. Lin Su

    Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8784-3120

  3. Gleb Pishchany

    Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.

  4. Moshe Baruch

    Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.

  5. Jose Cornejo

    Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.

  6. Elissa Hobert

    Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.

  7. Eric Dimise

    Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
    For correspondence
    ejdimise@gmail.com
    Competing interests
    No competing interests declared.

  8. Caroline M Ajo-Franklin

    Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.

  9. Jon Clardy

    Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
    For correspondence
    jon_clardy@hms.harvard.edu
    Competing interests
    Jon Clardy, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0213-8356

Funding

National Institute of General Medical Sciences (GM086258)

  • Jon Clardy

National Center for Complementary and Integrative Health (AT980074)

  • Jon Clardy

U.S. Department of Energy (DE-AC02-05CH11231)

  • Caroline M Ajo-Franklin

National Institute of General Medical Sciences (5F32GM103010)

  • Elissa Hobert

China Scholarship Council (201606090098)

  • Lin Su

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Dianne K Newman, California Institute of Technology, United States

Publication history

  1. Received: April 29, 2019
  2. Accepted: June 24, 2019
  3. Accepted Manuscript published: June 24, 2019 (version 1)
  4. Version of Record published: August 8, 2019 (version 2)

Copyright

© 2019, Mevers et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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