Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “CandidatusTenderia electrophaga”

Abstract

Bacteria that directly use electrodes as metabolic electron donors (biocathodes) have been proposed for applications ranging from microbial electrosynthesis to advanced bioelectronics for cellular communication with machines. However, just as we understand very little about oxidation of analogous natural insoluble electron donors, such as iron oxide, the organisms and extracellular electron transfer (EET) pathways underlying the electrode-cell direct electron transfer processes are almost completely unknown. Biocathodes are a stable biofilm cultivation platform to interrogate both the rate and mechanism of EET using electrochemistry and to study the electroautotrophic organisms that catalyze these reactions. Here we provide new evidence supporting the hypothesis that the uncultured bacterium “Candidatus Tenderia electrophaga” directly couples extracellular electron transfer to CO2 fixation. Our results provide insight into developing biocathode technology, such as microbial electrosynthesis, as well as advancing our understanding of chemolithoautotrophy.

The Effect of Oxygen Mass Transfer on Aerobic Biocathode Performance, Biofilm Growth and Distribution in Microbial Fuel Cells

“…Recently, a putative electron transport chain involving extracellular electron transfer for the electroautotroph ‘ Candidatus Tenderia electrophaga' was proposed based on metagenomics , metaproteomics , and metatranscriptomics studies . The findings suggest that electrons are accepted from the cathode electrode via an outer‐membrane bound cytochrome, similar to Cyc2 in iron oxidizing bacteria, and are utilized in downhill and uphill electron transport pathways , . In the downhill pathway, electrons are ultimately used to reduce oxygen to water via a terminal heme‐copper oxidase on the inner membrane, producing proton motive force for ATP synthesis via ATP synthase, whilst in the downhill pathway, electrons are transferred to a NADH:quinone oxidoreductase which catalyzes the production of NAD(P)H from NAD(P) + , .…”

“…The findings suggest that electrons are accepted from the cathode electrode via an outer‐membrane bound cytochrome, similar to Cyc2 in iron oxidizing bacteria, and are utilized in downhill and uphill electron transport pathways , . In the downhill pathway, electrons are ultimately used to reduce oxygen to water via a terminal heme‐copper oxidase on the inner membrane, producing proton motive force for ATP synthesis via ATP synthase, whilst in the downhill pathway, electrons are transferred to a NADH:quinone oxidoreductase which catalyzes the production of NAD(P)H from NAD(P) + , . The ATP and NAD(P)H which are generated can then be used to fix carbon dioxide into biomass via the Calvin‐Benson‐Bassham cycle .…”

“…This catalytic behavior is believed to be due to the activity of uncultured Gammaproteobacteria , , which likely gain energy for metabolism and growth by using electrons derived directly from the electrode, simultaneously catalyzing the ORR . Recently, a putative electron transport chain involving extracellular electron transfer for the electroautotroph ‘ Candidatus Tenderia electrophaga' was proposed based on metagenomics , metaproteomics , and metatranscriptomics studies . The findings suggest that electrons are accepted from the cathode electrode via an outer‐membrane bound cytochrome, similar to Cyc2 in iron oxidizing bacteria, and are utilized in downhill and uphill electron transport pathways , .…”

Electrochemical Characterization of Marinobacter atlanticus Strain CP1 Suggests a Role for Trace Minerals in Electrogenic Activity

“…The genome of M. atlanticus does not contain large multiheme c-type cytochromes, such as those known to facilitate EET in well-known electroactive (EA) organisms like Geobacter sulfurreducens (Otero et al, 2018) and Shewanella oneidensis MR1 (Coursolle et al, 2010). Features ascribed to an Fe-S 4containing protein were previously observed in the Biocathode MCL biofilm (Yates et al, 2016) and within the Biocathode MCL community M. atlanticus expresses the gene for rubredoxin (Eddie et al, 2017), a class of small Fe-S 4 proteins commonly involved in electron transfer events (Zanello, 2013;Liu et al, 2014). While rubredoxin has not yet been identified as a component of an EET conduit, synthetic biofilms employing rubredoxin as the charge mediator are capable of electron transfer between an electrode and a multi-copper enzyme and achieved even higher current densities than corresponding systems using cytochrome c (Altamura et al, 2017); therefore, its function as an ET mediator in M. atlanticus was explored.…”

Microbial succession during the transition from active to inactive stages of deep-sea hydrothermal vent sulfide chimneys

“…The prevalence of the cyc2 gene identified in their MAGs suggests that, besides sulfide, Fe 2+ from minerals (like pyrite and pyrrhotite) likely serves as an alternative electron donor for these autotrophs. This gene encodes an outer membrane cytochrome c, which was demonstrated to mediate iron oxidation in the acidophilic FeOB Acidithiobacillus ferrooxidans and has also been found in all available genomes of neutrophilic FeOB and has been proposed as a candidate genetic marker for FeOB [74,88,90]. Moreover, a highly expressed cyc2 gene identified in the electroautotrophic Ca.…”