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Tracking electron uptake from a cathode into Shewanella cells: implications for generating maintenance energy from solid substrates

Annette R. Rowe, Pournami Rajeev, Abhiney Jain, Sahand Pirbadian, Akihiro Okamotao, Jeffrey A. Gralnick, Mohamed Y. El-Naggar, Kenneth H. Nealson
doi: https://doi.org/10.1101/116475
Annette R. Rowe
aDepartment of Earth Sciences, University of Southern California, Los Angeles, CA, 90089
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Pournami Rajeev
aDepartment of Earth Sciences, University of Southern California, Los Angeles, CA, 90089
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Abhiney Jain
bDepartment of Microbiology and Biotechnology Institute, University of Minnesota, St. Paul, MN, 55108
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Sahand Pirbadian
cDepartment of Physics and Astronomy, University of Southern California, Los Angeles, CA, 90089
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Akihiro Okamotao
dGlobal Research Center for Environmental and Energy based on Nanomaterials Science, National Institute for Materials Science (NIMS), Tsukuba-city Ibaraki, Japan, 305-0047
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Jeffrey A. Gralnick
bDepartment of Microbiology and Biotechnology Institute, University of Minnesota, St. Paul, MN, 55108
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Mohamed Y. El-Naggar
cDepartment of Physics and Astronomy, University of Southern California, Los Angeles, CA, 90089
eDepartment of Biological Sciences, University of Southern California, Los Angeles, CA, 90089
fDepartment of Chemistry, University of Southern California, Los Angeles, CA, 90089
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Kenneth H. Nealson
aDepartment of Earth Sciences, University of Southern California, Los Angeles, CA, 90089
eDepartment of Biological Sciences, University of Southern California, Los Angeles, CA, 90089
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Abstract

While typically investigated as a microorganism capable of extracellular electron transfer to minerals or anodes, Shewanella oneidensis MR-1 can also facilitate electron flow from a cathode to terminal electron acceptors such as fumarate or oxygen, thereby providing a model systems for a process that has significant environmental and technological implications. This work demonstrates that cathodic electrons enter the electron transport chain of S. oneidensis when oxygen is used as the terminal electron acceptor. The effect of electron transport chain inhibitors suggested that a proton gradient is generated during cathode-oxidation, consistent with the higher cellular ATP levels measured in cathode-respiring cells relative to controls. Cathode oxidation also correlated with an increase in the cellular redox (NADH/FMNH2) pool using a bioluminescent assay. Using a proton uncoupler, generation of NADH/FMNH2 under cathodic conditions was linked to reverse electron flow mediated by the proton pumping NADH oxidase Complex I. A decrease in cathodic electron uptake was observed in various mutant strains including those lacking the extracellular electron transfer components necessary for anodic current generation. While no cell growth was observed under these conditions, here we show that cathode oxidation is linked to cellular energy conservation, resulting in a quantifiable reduction in cellular decay rate. This work highlights a potential mechanism for cell survival and/or persistence in environments where growth and division are severely limited.

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Posted March 14, 2017.
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Tracking electron uptake from a cathode into Shewanella cells: implications for generating maintenance energy from solid substrates
Annette R. Rowe, Pournami Rajeev, Abhiney Jain, Sahand Pirbadian, Akihiro Okamotao, Jeffrey A. Gralnick, Mohamed Y. El-Naggar, Kenneth H. Nealson
bioRxiv 116475; doi: https://doi.org/10.1101/116475
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Tracking electron uptake from a cathode into Shewanella cells: implications for generating maintenance energy from solid substrates
Annette R. Rowe, Pournami Rajeev, Abhiney Jain, Sahand Pirbadian, Akihiro Okamotao, Jeffrey A. Gralnick, Mohamed Y. El-Naggar, Kenneth H. Nealson
bioRxiv 116475; doi: https://doi.org/10.1101/116475

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