Title: Tracking Electron Uptake from a Cathode into Shewanella Cells: Implications for Energy Acquisition from Solid-Substrate Electron Donors

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 system for a process that has significant environmental and technological implications. This work demonstrates that cathodic electrons enter the electron transport chain ofS. oneidensiswhen 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 than in controls. Cathode oxidation also correlated with an increase in the cellular redox (NADH/FMNH₂) pool determined with a bioluminescence assay, a proton uncoupler, and a mutant of proton-pumping NADH oxidase complex I. This work suggested that the generation of NADH/FMNH₂ under cathodic conditions was linked to reverse electron flow mediated by 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 acquisition, resulting in a quantifiablemore » reduction in the cellular decay rate. This work highlights a potential mechanism for cell survival and/or persistence on cathodes, which might extend to environments where growth and division are severely limited. The majority of our knowledge of the physiology of extracellular electron transfer derives from studies of electrons moving to the exterior of the cell. The physiological mechanisms and/or consequences of the reverse processes are largely uncharacterized. This report demonstrates that when coupled to oxygen reduction, electrode oxidation can result in cellular energy acquisition. This respiratory process has potentially important implications for how microorganisms persist in energy-limited environments, such as reduced sediments under changing redox conditions. From an applied perspective, this work has important implications for microbially catalyzed processes on electrodes, particularly with regard to understanding models of cellular conversion of electrons from cathodes to microbially synthesized products.« less

Authors:

Rowe, Annette R. ^[1]; Rajeev, Pournami ^[1]; Jain, Abhiney ^[2]; Pirbadian, Sahand ^[3]; Okamoto, Akihiro ^[4]; Gralnick, Jeffrey A. ^[2]; El-Naggar, Mohamed Y. ^[5]; Nealson, Kenneth H. ^[6]

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+ Show Author Affiliations

1. Univ. of Southern California, Los Angeles, CA (United States). Dept. of Earth Sciences
2. Univ. of Minnesota, St. Paul, Minnesota (United States). Dept. of Microbiology, BioTechnology Inst.
3. Univ. of Minnesota, St. Paul, Minnesota (United States). Dept. of Physics and Astronomy
4. National Inst. for Materials Science (NIMS), Tsukuba (Japan). Global Research Center for Environment and Energy Based on Nanomaterials Science
5. Univ. of Minnesota, St. Paul, Minnesota (United States). Dept. of Physics and Astronomy; Univ. of Southern California, Los Angeles, CA (United States). Dept. of Dept. of Biological Sciences, Dept. of Chemistry
6. Univ. of Southern California, Los Angeles, CA (United States). Dept. of Earth Sciences, and Dept. of Biological Sciences

Publication Date:

Tue Feb 27 00:00:00 EST 2018

Research Org.:

Univ. of Southern California, Los Angeles, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:

1505196

Grant/Contract Number:  

SC0010609

Resource Type:

Accepted Manuscript

Journal Name:

mBio (Online)

Additional Journal Information:

Journal Name: mBio (Online); Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2150-7511

Publisher:

American Society for Microbiology

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; electron uptake; energy acquisition; reverse electron transport; Shewanella; systems biology