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Title: An elusive electron shuttle from a facultative anaerobe

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.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [4];  [1];  [1];  [5]; ORCiD logo [1]
  1. Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States
  2. Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States, State Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast University, Nanjing, China
  3. Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United States, Department of Microbiology, Harvard Medical School, Boston, United States
  4. Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States
  5. Molecular Foundry Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States, Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, Berkeley, United States
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1529030
Alternate Identifier(s):
OSTI ID: 1529031
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
eLife
Additional Journal Information:
Journal Name: eLife Journal Volume: 8; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English

Citation Formats

Mevers, Emily, Su, Lin, Pishchany, Gleb, Baruch, Moshe, Cornejo, Jose, Hobert, Elissa, Dimise, Eric, Ajo-Franklin, Caroline M., and Clardy, Jon. An elusive electron shuttle from a facultative anaerobe. United States: N. p., 2019. Web. doi:10.7554/eLife.48054.
Mevers, Emily, Su, Lin, Pishchany, Gleb, Baruch, Moshe, Cornejo, Jose, Hobert, Elissa, Dimise, Eric, Ajo-Franklin, Caroline M., & Clardy, Jon. An elusive electron shuttle from a facultative anaerobe. United States. doi:10.7554/eLife.48054.
Mevers, Emily, Su, Lin, Pishchany, Gleb, Baruch, Moshe, Cornejo, Jose, Hobert, Elissa, Dimise, Eric, Ajo-Franklin, Caroline M., and Clardy, Jon. Mon . "An elusive electron shuttle from a facultative anaerobe". United States. doi:10.7554/eLife.48054.
@article{osti_1529030,
title = {An elusive electron shuttle from a facultative anaerobe},
author = {Mevers, Emily and Su, Lin and Pishchany, Gleb and Baruch, Moshe and Cornejo, Jose and Hobert, Elissa and Dimise, Eric and Ajo-Franklin, Caroline M. and Clardy, Jon},
abstractNote = {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.},
doi = {10.7554/eLife.48054},
journal = {eLife},
number = ,
volume = 8,
place = {United States},
year = {2019},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.7554/eLife.48054

Citation Metrics:
Cited by: 2 works
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