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Title: An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9

Abstract

Extracellular electron transfer (EET) allows microbes to acquire energy from solid state electron acceptors and donors, such as environmental minerals. Here, this process can also be harnessed at electrode interfaces in bioelectrochemical technologies including microbial fuel cells, microbial electrosynthesis, bioremediation, and wastewater treatment. Improving the performance of these technologies will benefit from a better fundamental understanding of EET in diverse microbial systems. While the mechanisms of outward (i.e. microbe-to-anode) EET is relatively well characterized, specifically in a few metal-reducing bacteria, the reverse process of inward EET from redox-active minerals or cathodes to bacteria remains poorly understood. This knowledge gap stems, at least partly, from the lack of well-established model organisms and general difficulties associated with laboratory studies in existing model systems. Recently, a sulfur oxidizing marine microbe, Thioclava electrotropha ElOx9, was demonstrated to perform electron uptake from cathodes. However, a detailed analysis of the electron uptake pathways has yet to be established, and electrochemical characterization has been limited to aerobic conditions. Here, we report a detailed amperometric and voltammetric characterization of ElOx9 cells coupling cathodic electron uptake to reduction of nitrate as the sole electron acceptor, even in the absence of any added inorganic carbon source. By comparing this cellularmore » activity to spent media controls and using medium exchange experiments, we demonstrate that one of the pathways by which ElOx9 facilitates inward EET is by a direct-contact mechanism through a redox center with a formal potential of -94 mV vs SHE, rather than soluble intermediate electron carriers. In addition to the implications for understanding microbial sulfur oxidation in marine environments, this study highlights the potential for ElOx9 to serve as a convenient and readily culturable model organism for understanding the molecular mechanisms of inward EET.« less

Authors:
 [1];  [2];  [1]
  1. Univ. of Southern California, Los Angeles, CA (United States)
  2. Univ. of Cincinnati, OH (United States)
Publication Date:
Research Org.:
Univ. of Southern California, Los Angeles, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF); National Aeronautics and Space Administration (NASA); USDOE
OSTI Identifier:
1802137
Alternate Identifier(s):
OSTI ID: 1562180
Grant/Contract Number:  
SC0010609; FG02-13ER16415; DEB-1542527; NNA13AA92A; NSF-STC OCE0939564
Resource Type:
Accepted Manuscript
Journal Name:
Electrochimica Acta
Additional Journal Information:
Journal Volume: 324; Journal Issue: C; Journal ID: ISSN 0013-4686
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; electrochemistry; electromicrobiology; extracellular electron transfer; lithotrophy; biocathodes

Citation Formats

Karbelkar, Amruta A., Rowe, Annette R., and El-Naggar, Mohamed Y. An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9. United States: N. p., 2019. Web. doi:10.1016/j.electacta.2019.134838.
Karbelkar, Amruta A., Rowe, Annette R., & El-Naggar, Mohamed Y. An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9. United States. https://doi.org/10.1016/j.electacta.2019.134838
Karbelkar, Amruta A., Rowe, Annette R., and El-Naggar, Mohamed Y. Fri . "An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9". United States. https://doi.org/10.1016/j.electacta.2019.134838. https://www.osti.gov/servlets/purl/1802137.
@article{osti_1802137,
title = {An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9},
author = {Karbelkar, Amruta A. and Rowe, Annette R. and El-Naggar, Mohamed Y.},
abstractNote = {Extracellular electron transfer (EET) allows microbes to acquire energy from solid state electron acceptors and donors, such as environmental minerals. Here, this process can also be harnessed at electrode interfaces in bioelectrochemical technologies including microbial fuel cells, microbial electrosynthesis, bioremediation, and wastewater treatment. Improving the performance of these technologies will benefit from a better fundamental understanding of EET in diverse microbial systems. While the mechanisms of outward (i.e. microbe-to-anode) EET is relatively well characterized, specifically in a few metal-reducing bacteria, the reverse process of inward EET from redox-active minerals or cathodes to bacteria remains poorly understood. This knowledge gap stems, at least partly, from the lack of well-established model organisms and general difficulties associated with laboratory studies in existing model systems. Recently, a sulfur oxidizing marine microbe, Thioclava electrotropha ElOx9, was demonstrated to perform electron uptake from cathodes. However, a detailed analysis of the electron uptake pathways has yet to be established, and electrochemical characterization has been limited to aerobic conditions. Here, we report a detailed amperometric and voltammetric characterization of ElOx9 cells coupling cathodic electron uptake to reduction of nitrate as the sole electron acceptor, even in the absence of any added inorganic carbon source. By comparing this cellular activity to spent media controls and using medium exchange experiments, we demonstrate that one of the pathways by which ElOx9 facilitates inward EET is by a direct-contact mechanism through a redox center with a formal potential of -94 mV vs SHE, rather than soluble intermediate electron carriers. In addition to the implications for understanding microbial sulfur oxidation in marine environments, this study highlights the potential for ElOx9 to serve as a convenient and readily culturable model organism for understanding the molecular mechanisms of inward EET.},
doi = {10.1016/j.electacta.2019.134838},
journal = {Electrochimica Acta},
number = C,
volume = 324,
place = {United States},
year = {Fri Sep 06 00:00:00 EDT 2019},
month = {Fri Sep 06 00:00:00 EDT 2019}
}

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Works referenced in this record:

Performance of different Sporomusa species for the microbial electrosynthesis of acetate from carbon dioxide
journal, June 2017


Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency
journal, January 2007

  • Schröder, Uwe
  • Phys. Chem. Chem. Phys., Vol. 9, Issue 21
  • DOI: 10.1039/B703627M

Electron uptake by iron-oxidizing phototrophic bacteria
journal, February 2014

  • Bose, A.; Gardel, E. J.; Vidoudez, C.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4391

Extracellular respiration
journal, July 2007


Anodic and Cathodic Extracellular Electron Transfer by the Filamentous Bacterium Ardenticatena maritima 110S
journal, February 2018


Enhanced Alcaligenes faecalis Denitrification Rate with Electrodes as the Electron Donor
journal, June 2015

  • Wang, Xin; Yu, Ping; Zeng, Cuiping
  • Applied and Environmental Microbiology, Vol. 81, Issue 16
  • DOI: 10.1128/AEM.00683-15

Microbial Electroreduction: Screening for New Cathodic Biocatalysts
journal, September 2014

  • de Campos Rodrigues, Tatiana; Rosenbaum, Miriam A.
  • ChemElectroChem, Vol. 1, Issue 11
  • DOI: 10.1002/celc.201402239

Extracellular Electron Uptake: Among Autotrophs and Mediated by Surfaces
journal, April 2017


Tracking Electron Uptake from a Cathode into Shewanella Cells: Implications for Energy Acquisition from Solid-Substrate Electron Donors
journal, February 2018


Secretion of Flavins by Shewanella Species and Their Role in Extracellular Electron Transfer
journal, December 2007

  • von Canstein, H.; Ogawa, J.; Shimizu, S.
  • Applied and Environmental Microbiology, Vol. 74, Issue 3
  • DOI: 10.1128/AEM.01387-07

Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
journal, April 2015

  • Deutzmann, Jörg S.; Sahin, Merve; Spormann, Alfred M.
  • mBio, Vol. 6, Issue 2
  • DOI: 10.1128/mBio.00496-15

Isolation and Characterization of Electrochemically Active Subsurface Delftia and Azonexus Species
journal, May 2016


Cultivation of an Obligate Fe(II)-Oxidizing Lithoautotrophic Bacterium Using Electrodes
journal, January 2013

  • Summers, Zarath M.; Gralnick, Jeffrey A.; Bond, Daniel R.
  • mBio, Vol. 4, Issue 1
  • DOI: 10.1128/mBio.00420-12

Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms
journal, October 2008

  • Marsili, E.; Rollefson, J. B.; Baron, D. B.
  • Applied and Environmental Microbiology, Vol. 74, Issue 23
  • DOI: 10.1128/AEM.00177-08

Electron transfer at the microbe–mineral interface: a grand challenge in biogeochemistry
journal, June 2008


Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities
journal, January 2015

  • Breuer, Marian; Rosso, Kevin M.; Blumberger, Jochen
  • Journal of The Royal Society Interface, Vol. 12, Issue 102
  • DOI: 10.1098/rsif.2014.1117

Inhibition, but not uncoupling, of respiratory energy coupling of three bacterial species by nitrite.
journal, January 1980


Voltammetry and Growth Physiology of Geobacter sulfurreducens Biofilms as a Function of Growth Stage and Imposed Electrode Potential
journal, March 2010

  • Marsili, Enrico; Sun, Jian; Bond, Daniel R.
  • Electroanalysis, Vol. 22, Issue 7-8
  • DOI: 10.1002/elan.200800007

A combined electrochemical and optical trapping platform for measuring single cell respiration rates at electrode interfaces
journal, June 2015

  • Gross, Benjamin J.; El-Naggar, Mohamed Y.
  • Review of Scientific Instruments, Vol. 86, Issue 6
  • DOI: 10.1063/1.4922853

Electrochemical growth of Acidithiobacillus ferrooxidans on a graphite electrode for obtaining a biocathode for direct electrocatalytic reduction of oxygen
journal, October 2010

  • Carbajosa, Sofía; Malki, Moustafá; Caillard, Renaud
  • Biosensors and Bioelectronics, Vol. 26, Issue 2
  • DOI: 10.1016/j.bios.2010.07.037

Prokaryotic Nitrate Reduction: Molecular Properties and Functional Distinction among Bacterial Nitrate Reductases
journal, November 1999


Microbial Electrosynthesis: Feeding Microbes Electricity To Convert Carbon Dioxide and Water to Multicarbon Extracellular Organic Compounds
journal, May 2010

  • Nevin, K. P.; Woodard, T. L.; Franks, A. E.
  • mBio, Vol. 1, Issue 2, Article No. e00103-10
  • DOI: 10.1128/mBio.00103-10

Towards Electrosynthesis in Shewanella: Energetics of Reversing the Mtr Pathway for Reductive Metabolism
journal, February 2011


Direct Biological Conversion of Electrical Current into Methane by Electromethanogenesis
journal, May 2009

  • Cheng, Shaoan; Xing, Defeng; Call, Douglas F.
  • Environmental Science & Technology, Vol. 43, Issue 10, p. 3953-3958
  • DOI: 10.1021/es803531g

Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1
journal, October 2010

  • El-Naggar, M. Y.; Wanger, G.; Leung, K. M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 42
  • DOI: 10.1073/pnas.1004880107

Direct uptake of electrode electrons for autotrophic denitrification by Thiobacillus denitrificans
journal, November 2015


Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1
journal, April 2016


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


Electron Extraction from an Extracellular Electrode by Desulfovibrio ferrophilus Strain IS5 Without Using Hydrogen as an Electron Carrier
journal, January 2015


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

Genome sequence of the dissimilatory metal ion–reducing bacterium Shewanella oneidensis
journal, October 2002

  • Heidelberg, John F.; Paulsen, Ian T.; Nelson, Karen E.
  • Nature Biotechnology, Vol. 20, Issue 11
  • DOI: 10.1038/nbt749

Microbial electrolysis cell platform for simultaneous waste biorefinery and clean electrofuels generation: Current situation, challenges and future perspectives
journal, November 2017

  • Zhen, Guangyin; Lu, Xueqin; Kumar, Gopalakrishnan
  • Progress in Energy and Combustion Science, Vol. 63
  • DOI: 10.1016/j.pecs.2017.07.003

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

Extracellular electron transfer via microbial nanowires
journal, June 2005

  • Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena
  • Nature, Vol. 435, Issue 7045, p. 1098-1101
  • DOI: 10.1038/nature03661

Thioclava electrotropha sp. nov., a versatile electrode and sulfur-oxidizing bacterium from marine sediments
journal, May 2018

  • Chang, Rachel; Bird, Lina; Barr, Casey
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 5
  • DOI: 10.1099/ijsem.0.002723

Cathodes as electron donors for microbial metabolism: Which extracellular electron transfer mechanisms are involved?
journal, January 2011