DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1529030
Alternate Identifier(s):
OSTI ID: 1529031; OSTI ID: 1628909
Grant/Contract Number:  
AC02-05CH11231; 201606090098; N0001419IP00023; 5F32GM103010
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
Subject:
59 BASIC BIOLOGICAL SCIENCES; Life Sciences & Biomedicine - Other Topics

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. https://doi.org/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. https://doi.org/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 = {Mon Jun 24 00:00:00 EDT 2019},
month = {Mon Jun 24 00:00:00 EDT 2019}
}

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

Citation Metrics:
Cited by: 35 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Rapid construction of a whole-genome transposon insertion collection for Shewanella oneidensis by Knockout Sudoku
journal, November 2016

  • Baym, Michael; Shaket, Lev; Anzai, Isao A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13270

Genetic identification of a respiratory arsenate reductase
journal, August 2003

  • Saltikov, C. W.; Newman, D. K.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 19
  • DOI: 10.1073/pnas.1834303100

Extracellular respiration
journal, July 2007


A role for excreted quinones in extracellular electron transfer
journal, May 2000

  • Newman, Dianne K.; Kolter, Roberto
  • Nature, Vol. 405, Issue 6782
  • DOI: 10.1038/35011098

Reconstruction of Extracellular Respiratory Pathways for Iron(III) Reduction in Shewanella Oneidensis Strain MR-1
journal, January 2012


Voltammetric Characterization of DNA Intercalators across the Full pH Range: Anthraquinone-2,6-disulfonate and Anthraquinone-2-sulfonate
journal, March 2010

  • Batchelor-McAuley, Christopher; Li, Qian; Dapin, Sophie M.
  • The Journal of Physical Chemistry B, Vol. 114, Issue 11
  • DOI: 10.1021/jp1008187

A Novel Bifidogenic Growth Stimulator Produced by Propionibacterium freudenreichii
journal, January 1999


Isolation and Structural Identification of Bifidogenic Growth Stimulator Produced by Propionibacterium freudenreichii
journal, September 1997


Bacterial Manganese Reduction and Growth with Manganese Oxide as the Sole Electron Acceptor
journal, June 1988


Production of extracellular bifidogenic growth stimulator by anaerobic and aerobic cultivations of several propionibacterial strains
journal, May 2007

  • Kouya, Tomoaki; Misawa, Katsuhiro; Horiuchi, Masahito
  • Journal of Bioscience and Bioengineering, Vol. 103, Issue 5
  • DOI: 10.1263/jbb.103.464

Extracellular electron transfer mechanisms between microorganisms and minerals
journal, August 2016

  • Shi, Liang; Dong, Hailiang; Reguera, Gemma
  • Nature Reviews Microbiology, Vol. 14, Issue 10
  • DOI: 10.1038/nrmicro.2016.93

METLIN: A Technology Platform for Identifying Knowns and Unknowns
journal, January 2018

  • Guijas, Carlos; Montenegro-Burke, J. Rafael; Domingo-Almenara, Xavier
  • Analytical Chemistry, Vol. 90, Issue 5
  • DOI: 10.1021/acs.analchem.7b04424

Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella
journal, November 2011

  • Brutinel, Evan D.; Gralnick, Jeffrey A.
  • Applied Microbiology and Biotechnology, Vol. 93, Issue 1
  • DOI: 10.1007/s00253-011-3653-0

Shewanella secretes flavins that mediate extracellular electron transfer
journal, March 2008

  • Marsili, E.; Baron, D. B.; Shikhare, I. D.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 10
  • DOI: 10.1073/pnas.0710525105

Works referencing / citing this record:

Interdependency of Respiratory Metabolism and Phenazine-Associated Physiology in Pseudomonas aeruginosa PA14
journal, November 2019

  • Jo, Jeanyoung; Price-Whelan, Alexa; Cornell, William Cole
  • Journal of Bacteriology, Vol. 202, Issue 4
  • DOI: 10.1128/jb.00700-19

Solving a shuttle mystery
journal, August 2019