An elusive electron shuttle from a facultative anaerobe

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Cite this article as: eLife 2019;8:e48054 doi: 10.7554/eLife.48054

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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 V_Ag/AgCl) contributes to the extracellular electron transfer (EET) as an electron shuttle, without altering menaquinone generation or EET related cytochrome c expression.

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Author details

Emily Mevers

Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-7986-5610
Lin Su

Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-8784-3120
Gleb Pishchany

Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States

Competing interests
No competing interests declared.
Moshe Baruch

Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Jose Cornejo

Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Elissa Hobert

Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States

Competing interests
No competing interests declared.
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.
Caroline M Ajo-Franklin

Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
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.

"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

Dianne K Newman, California Institute of Technology, United States

Publication history

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

Copyright

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.