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      [NiFe]-hydrogenases are constitutively expressed in an enriched Methanobacterium sp. population during electromethanogenesis

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          Abstract

          Electromethanogenesis is the bioreduction of carbon dioxide (CO 2) to methane (CH 4) utilizing an electrode as electron donor. Some studies have reported the active participation of Methanobacterium sp. in electron capturing, although no conclusive results are available. In this study, we aimed at determining short-time changes in the expression levels of [NiFe]-hydrogenases (Eha, Ehb and Mvh), heterodisulfide reductase (Hdr), coenzyme F 420-reducing [NiFe]-hydrogenase (Frh), and hydrogenase maturation protein (HypD), according to the electron flow in independently connected carbon cloth cathodes poised at– 800 mV vs. standard hydrogen electrode (SHE). Amplicon massive sequencing of cathode biofilm confirmed the presence of an enriched Methanobacterium sp. population (>70% of sequence reads), which remained in an active state (78% of cDNA reads), tagging this archaeon as the main methane producer in the system. Quantitative RT-PCR determinations of ehaB, ehbL, mvhA, hdrA, frhA, and hypD genes resulted in only slight (up to 1.5 fold) changes for four out of six genes analyzed when cells were exposed to open (disconnected) or closed (connected) electric circuit events. The presented results suggested that suspected mechanisms for electron capturing were not regulated at the transcriptional level in Methanobacterium sp. for short time exposures of the cells to connected-disconnected circuits. Additional tests are needed in order to confirm proteins that participate in electron capturing in Methanobacterium sp.

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          Direct biological conversion of electrical current into methane by electromethanogenesis.

          New sustainable methods are needed to produce renewable energy carriers that can be stored and used for transportation, heating, or chemical production. Here we demonstrate that methane can directly be produced using a biocathode containing methanogens in electrochemical systems (abiotic anode) or microbial electrolysis cells (MECs; biotic anode) by a process called electromethanogenesis. At a set potential of less than -0.7 V (vs Ag/AgCl), carbon dioxide was reduced to methane using a two-chamber electrochemical reactor containing an abiotic anode, a biocathode, and no precious metal catalysts. At -1.0 V, the current capture efficiency was 96%. Electrochemical measurements made using linear sweep voltammetry showed that the biocathode substantially increased current densities compared to a plain carbon cathode where only small amounts of hydrogen gas could be produced. Both increased current densities and very small hydrogen production rates by a plain cathode therefore support a mechanism of methane production directly from current and not from hydrogen gas. The biocathode was dominated by a single Archaeon, Methanobacterium palustre. When a current was generated by an exoelectrogenic biofilm on the anode growing on acetate in a single-chamber MEC, methane was produced at an overall energy efficiency of 80% (electrical energy and substrate heat of combustion). These results show that electromethanogenesis can be used to convert electrical current produced from renewable energy sources (such as wind, solar, or biomass) into a biofuel (methane) as well as serving as a method for the capture of carbon dioxide.
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            Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri.

            Direct interspecies electron transfer (DIET) is potentially an effective form of syntrophy in methanogenic communities, but little is known about the diversity of methanogens capable of DIET. The ability of Methanosarcina barkeri to participate in DIET was evaluated in coculture with Geobacter metallireducens. Cocultures formed aggregates that shared electrons via DIET during the stoichiometric conversion of ethanol to methane. Cocultures could not be initiated with a pilin-deficient G. metallireducens strain, suggesting that long-range electron transfer along pili was important for DIET. Amendments of granular activated carbon permitted the pilin-deficient G. metallireducens isolates to share electrons with M. barkeri, demonstrating that this conductive material could substitute for pili in promoting DIET. When M. barkeri was grown in coculture with the H2-producing Pelobacter carbinolicus, incapable of DIET, M. barkeri utilized H2 as an electron donor but metabolized little of the acetate that P.carbinolicus produced. This suggested that H2, but not electrons derived from DIET, inhibited acetate metabolism. P. carbinolicus-M. barkeri cocultures did not aggregate, demonstrating that, unlike DIET, close physical contact was not necessary for interspecies H2 transfer. M. barkeri is the second methanogen found to accept electrons via DIET and the first methanogen known to be capable of using either H2 or electrons derived from DIET for CO2 reduction. Furthermore, M. barkeri is genetically tractable,making it a model organism for elucidating mechanisms by which methanogens make biological electrical connections with other cells.
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              Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage.

              Most methanogenic archaea reduce CO(2) with H(2) to CH(4). For the activation of H(2), they use different [NiFe]-hydrogenases, namely energy-converting [NiFe]-hydrogenases, heterodisulfide reductase-associated [NiFe]-hydrogenase or methanophenazine-reducing [NiFe]-hydrogenase, and F(420)-reducing [NiFe]-hydrogenase. The energy-converting [NiFe]-hydrogenases are phylogenetically related to complex I of the respiratory chain. Under conditions of nickel limitation, some methanogens synthesize a nickel-independent [Fe]-hydrogenase (instead of F(420)-reducing [NiFe]-hydrogenase) and by that reduce their nickel requirement. The [Fe]-hydrogenase harbors a unique iron-guanylylpyridinol cofactor (FeGP cofactor), in which a low-spin iron is ligated by two CO, one C(O)CH(2)-, one S-CH(2)-, and a sp(2)-hybridized pyridinol nitrogen. Ligation of the iron is thus similar to that of the low-spin iron in the binuclear active-site metal center of [NiFe]- and [FeFe]-hydrogenases. Putative genes for the synthesis of the FeGP cofactor have been identified. The formation of methane from 4 H(2) and CO(2) catalyzed by methanogenic archaea is being discussed as an efficient means to store H(2).
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                11 April 2019
                2019
                : 14
                : 4
                : e0215029
                Affiliations
                [1 ] Molecular Microbial Ecology Group, Institute of Aquatic Ecology, University of Girona, Girona, Spain
                [2 ] LEQUiA, Institute of the Environment, University of Girona, Girona, Spain
                Universidade Nova de Lisboa Instituto de Tecnologia Quimica e Biologica, PORTUGAL
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-6000-069X
                http://orcid.org/0000-0001-6908-3658
                Article
                PONE-D-18-36361
                10.1371/journal.pone.0215029
                6459506
                30973887
                11e941cb-bda9-4d6e-b7c0-f931f6537e37
                © 2019 Perona-Vico et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 20 December 2018
                : 25 March 2019
                Page count
                Figures: 4, Tables: 2, Pages: 16
                Funding
                Funded by: Ministerio de Economía, Industria y Competitividad, Gobierno de España (ES)
                Award ID: CTQ2014-53718-R
                Award Recipient :
                Funded by: Universitat de Girona
                Award ID: MPCUdG2016/139
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008722, Universitat de Girona;
                Award ID: MCPUdG2016/121
                Funded by: funder-id http://dx.doi.org/10.13039/501100003030, Agència de Gestió d’Ajuts Universitaris i de Recerca;
                Award ID: 2017SGR-1552
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003030, Agència de Gestió d’Ajuts Universitaris i de Recerca;
                Award ID: 2017SGR-548
                The Spanish Government (MINECO http://www.mineco.gob.es/) contributed trough project BioGasApp (CTQ2014-53718-R). Universitat de Girona ( https://www.udg.edu) contributed through projects MPCUdG2016/139 to JC and MCPUdG2016/121 to LB. R B-G received a Research Personnel Training (FPI) grant (BES-2015-074229). E P-V is recipient of a PhD grant from University of Girona ( https://www.udg.edu). S P is a Serra-Húnter Fellow (UdG-AG-575). Generalitat de Catalunya ( http://agaur.gencat.cat/) contributed through grants 2017SGR-1552 to RBG, JC and SP, and 2017SGR-548 to LB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Engineering and Technology
                Electronics
                Electrodes
                Cathodes
                Physical Sciences
                Chemistry
                Chemical Elements
                Hydrogen
                Biology and Life Sciences
                Microbiology
                Biofilms
                Earth Sciences
                Atmospheric Science
                Atmospheric Chemistry
                Greenhouse Gases
                Carbon Dioxide
                Physical Sciences
                Chemistry
                Environmental Chemistry
                Atmospheric Chemistry
                Greenhouse Gases
                Carbon Dioxide
                Ecology and Environmental Sciences
                Environmental Chemistry
                Atmospheric Chemistry
                Greenhouse Gases
                Carbon Dioxide
                Physical Sciences
                Chemistry
                Chemical Compounds
                Carbon Dioxide
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Databases
                Biology and Life Sciences
                Genetics
                Gene Expression
                Research and analysis methods
                Extraction techniques
                RNA extraction
                Earth Sciences
                Atmospheric Science
                Atmospheric Chemistry
                Greenhouse Gases
                Methane
                Physical Sciences
                Chemistry
                Environmental Chemistry
                Atmospheric Chemistry
                Greenhouse Gases
                Methane
                Ecology and Environmental Sciences
                Environmental Chemistry
                Atmospheric Chemistry
                Greenhouse Gases
                Methane
                Physical Sciences
                Chemistry
                Chemical Compounds
                Methane
                Custom metadata
                The sequences presented in this study have been submitted to the GenBank database within the SRA accession number SRP153784 (BioProject ID PRJNA481232). All other relevant data is included in the manuscript and its Supporting Information files.

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