Flavin Redox Bifurcation as a Mechanism for Controlling the Direction of Electron Flow during Extracellular Electron Transfer

2014 ◽  
Vol 126 (41) ◽  
pp. 11168-11171 ◽  
Author(s):  
Akihiro Okamoto ◽  
Kazuhito Hashimoto ◽  
Kenneth H. Nealson
Keyword(s):  
Electron Transfer ◽  
Electron Flow ◽  
Extracellular Electron Transfer

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

mBio ◽  
2018 ◽  
Vol 9 (1) ◽  
Author(s):  
Annette R. Rowe ◽  
Pournami Rajeev ◽  
Abhiney Jain ◽  
Sahand Pirbadian ◽  
Akihiro Okamoto ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electron Transport ◽  
Complex I ◽  
Electron Transport Chain ◽  
Electron Flow ◽  
Extracellular Electron Transfer ◽  
Terminal Electron Acceptor ◽  
Cellular Energy ◽  
Transport Chain ◽  
Energy Acquisition

ABSTRACTWhile typically investigated as a microorganism capable of extracellular electron transfer to minerals or anodes,Shewanella oneidensisMR-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/FMNH2under 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 quantifiable 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.IMPORTANCEThe 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.

scholarly journals Tracking electron uptake from a cathode intoShewanellacells: implications for generating maintenance energy from solid substrates

2017 ◽  
Author(s):  
Annette R. Rowe ◽  
Pournami Rajeev ◽  
Abhiney Jain ◽  
Sahand Pirbadian ◽  
Akihiro Okamotao ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electron Transport ◽  
Electron Transport Chain ◽  
Nadh Oxidase ◽  
Electron Flow ◽  
Proton Pumping ◽  
Model Systems ◽  
Extracellular Electron Transfer ◽  
Terminal Electron Acceptor ◽  
Transport Chain

While typically investigated as a microorganism capable of extracellular electron transfer to minerals or anodes,Shewanella oneidensisMR-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.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 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/FMNH2under 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.

scholarly journals Modeling biofilms with dual extracellular electron transfer mechanisms

2013 ◽  
Vol 15 (44) ◽  
pp. 19262 ◽  
Author(s):  
Ryan Renslow ◽  
Jerome Babauta ◽  
Andrew Kuprat ◽  
Jim Schenk ◽  
Cornelius Ivory ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Extracellular Electron Transfer ◽  
Transfer Mechanisms

scholarly journals Using Structure-Function Relationships to Understand the Mechanism of Phenazine Mediated Extracellular Electron Transfer in Escherichia coli

iScience ◽  
2021 ◽  
pp. 103033
Author(s):  
Zayn Rhodes ◽  
Olja Simoska ◽  
Ashwini Dantanarayana ◽  
Keith J. Stevenson ◽  
Shelley D. Minteer
Keyword(s):  
Escherichia Coli ◽  
Electron Transfer ◽  
Structure Function ◽  
Extracellular Electron Transfer

scholarly journals Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes

mSphere ◽  
2017 ◽  
Vol 2 (5) ◽  
Author(s):  
Shaomei He ◽  
Sarah L. R. Stevens ◽  
Leong-Keat Chan ◽  
Stefan Bertilsson ◽  
Tijana Glavina del Rio ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Potential Role ◽  
Carbon Sources ◽  
Genomic Analysis ◽  
Distribution Patterns ◽  
Eutrophic Lake ◽  
Genomic Diversity ◽  
Extracellular Electron Transfer ◽  
Different Origins ◽  
Encoding Genes

ABSTRACT Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. Here, we greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling. Microbes are critical in carbon and nutrient cycling in freshwater ecosystems. Members of the Verrucomicrobia are ubiquitous in such systems, and yet their roles and ecophysiology are not well understood. In this study, we recovered 19 Verrucomicrobia draft genomes by sequencing 184 time-series metagenomes from a eutrophic lake and a humic bog that differ in carbon source and nutrient availabilities. These genomes span four of the seven previously defined Verrucomicrobia subdivisions and greatly expand knowledge of the genomic diversity of freshwater Verrucomicrobia. Genome analysis revealed their potential role as (poly)saccharide degraders in freshwater, uncovered interesting genomic features for this lifestyle, and suggested their adaptation to nutrient availabilities in their environments. Verrucomicrobia populations differ significantly between the two lakes in glycoside hydrolase gene abundance and functional profiles, reflecting the autochthonous and terrestrially derived allochthonous carbon sources of the two ecosystems, respectively. Interestingly, a number of genomes recovered from the bog contained gene clusters that potentially encode a novel porin-multiheme cytochrome c complex and might be involved in extracellular electron transfer in the anoxic humus-rich environment. Notably, most epilimnion genomes have large numbers of so-called “Planctomycete-specific” cytochrome c-encoding genes, which exhibited distribution patterns nearly opposite to those seen with glycoside hydrolase genes, probably associated with the different levels of environmental oxygen availability and carbohydrate complexity between lakes/layers. Overall, the recovered genomes represent a major step toward understanding the role, ecophysiology, and distribution of Verrucomicrobia in freshwater. IMPORTANCE Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. Here, we greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling.

Geobacter sulfurreducens adapts to low electrode potential for extracellular electron transfer

2016 ◽  
Vol 191 ◽  
pp. 743-749 ◽  
Author(s):  
Luo Peng ◽  
Xiao-Ting Zhang ◽  
Jie Yin ◽  
Shuo-Yuan Xu ◽  
Yong Zhang ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electrode Potential ◽  
Geobacter Sulfurreducens ◽  
Extracellular Electron Transfer
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