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      Several ways one goal—methanogenesis from unconventional substrates

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          Abstract

          Abstract

          Methane is the second most important greenhouse gas on earth. It is produced by methanogenic archaea, which play an important role in the global carbon cycle. Three main methanogenesis pathways are known: in the hydrogenotrophic pathway H 2 and carbon dioxide are used for methane production, whereas in the methylotrophic pathway small methylated carbon compounds like methanol and methylated amines are used. In the aceticlastic pathway, acetate is disproportionated to methane and carbon dioxide. However, next to these conventional substrates, further methanogenic substrates and pathways have been discovered. Several phylogenetically distinct methanogenic lineages ( Methanosphaera, Methanimicrococcus, Methanomassiliicoccus, Methanonatronarchaeum) have evolved hydrogen-dependent methylotrophic methanogenesis without the ability to perform either hydrogenotrophic or methylotrophic methanogenesis. Genome analysis of the deep branching Methanonatronarchaeum revealed an interesting membrane-bound hydrogenase complex affiliated with the hardly described class 4 g of multisubunit hydrogenases possibly providing reducing equivalents for anabolism. Furthermore, methylated sulfur compounds such as methanethiol, dimethyl sulfide, and methylmercaptopropionate were described to be converted into adapted methylotrophic methanogenesis pathways of Methanosarcinales strains. Moreover, recently it has been shown that the methanogen Methermicoccus shengliensis can use methoxylated aromatic compounds in methanogenesis. Also, tertiary amines like choline ( N, N, N-trimethylethanolamine) or betaine ( N, N, N-trimethylglycine) have been described as substrates for methane production in Methanococcoides and Methanolobus strains. This review article will provide in-depth information on genome-guided metabolic reconstructions, physiology, and biochemistry of these unusual methanogenesis pathways.

          Key points

          Newly discovered methanogenic substrates and pathways are reviewed for the first time.

          • The review provides an in-depth analysis of unusual methanogenesis pathways.

          • The hydrogenase complex of the deep branching Methanonatronarchaeum is analyzed.

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          Most cited references72

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          Methanogenic archaea: ecologically relevant differences in energy conservation.

          Most methanogenic archaea can reduce CO(2) with H(2) to methane, and it is generally assumed that the reactions and mechanisms of energy conservation that are involved are largely the same in all methanogens. However, this does not take into account the fact that methanogens with cytochromes have considerably higher growth yields and threshold concentrations for H(2) than methanogens without cytochromes. These and other differences can be explained by the proposal outlined in this Review that in methanogens with cytochromes, the first and last steps in methanogenesis from CO(2) are coupled chemiosmotically, whereas in methanogens without cytochromes, these steps are energetically coupled by a cytoplasmic enzyme complex that mediates flavin-based electron bifurcation.
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            The global methane cycle: recent advances in understanding the microbial processes involved.

            The global budget of atmospheric CH4 , which is on the order of 500-600 Tg CH4 per year, is mainly the result of environmental microbial processes, such as archaeal methanogenesis in wetlands, rice fields, ruminant and termite digestive systems and of microbial methane oxidation under anoxic and oxic conditions. This review highlights recent progress in the research of anaerobic CH4 oxidation, of CH4 production in the plant rhizosphere, of CH4 serving as substrate for the aquatic trophic food chain and the discovery of novel aerobic methanotrophs. It also emphasizes progress and deficiencies in our knowledge of microbial utilization of low atmospheric CH4 concentrations in soil, CH4 production in the plant canopy, intestinal methanogenesis and CH4 production in pelagic water. © 2009 Society for Applied Microbiology and Blackwell Publishing Ltd.
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              Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces.

              During attempts to obtain novel, human-associated species of the domain Archaea, a coccoid micro-organism, designated strain B10(T), was isolated in pure culture from a sample of human faeces collected in Marseille, France. On the basis of its phenotypic characteristics and 16S rRNA and mcrA gene sequences, the novel strain was classified as a methanogenic archaeon. Cells of the strain were non-motile, Gram-staining-positive cocci that were approximately 850 nm in diameter and showed autofluorescence at 420 nm. Cells were lysed by 0.1% (w/v) SDS. With hydrogen as the electron donor, strain B10(T) produced methane by reducing methanol. The novel strain was unable to produce methane when hydrogen or methanol was the sole energy source. In an atmosphere containing CO(2), strain B10(T) could not produce methane from formate, acetate, trimethylamine, 2-butanol, 2-propanol, cyclopentanol, 2-pentanol, ethanol, 1-propanol or 2,3-butanediol. Strain B10(T) grew optimally with 0.5-1.0% (w/v) NaCl, at pH 7.6 and at 37 °C. It required tungstate-selenite for growth. The complete genome of the novel strain was sequenced; the size of the genome was estimated to be 2.05 Mb and the genomic DNA G+C content was 59.93 mol%. In phylogenetic analyses based on 16S rRNA gene sequences, the highest sequence similarities (98.0-98.7%) were seen between strain B10(T) and several uncultured, methanogenic Archaea that had been collected from the digestive tracts of a cockroach, a chicken and mammals. In the same analysis, the non-methanogenic 'Candidatus Aciduliprofundum boonei' DSM 19572 was identified as the cultured micro-organism that was most closely related to strain B10(T) (83.0% 16S rRNA gene sequence similarity). Each of the three treeing algorithms used in the analysis of 16S rRNA gene sequences indicated that strain B10(T) belongs to a novel order that is distinct from the Thermoplasmatales. The novel strain also appeared to be distinct from Methanosphaera stadtmanae DSM 3091(T) (72.9% 16S rRNA gene sequence similarity), another methanogenic archaeon that was isolated from human faeces and can use methanol in the presence of hydrogen. Based on the genetic and phenotypic evidence, strain B10(T) represents a novel species of a new genus for which the name Methanomassiliicoccus luminyensis gen. nov., sp. nov. is proposed. The type strain of the type species is B10(T) ( = DSM 24529(T) = CSUR P135(T)).
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                Author and article information

                Contributors
                h.opdencamp@science.ru.nl
                c.welte@science.ru.nl
                Journal
                Appl Microbiol Biotechnol
                Appl. Microbiol. Biotechnol
                Applied Microbiology and Biotechnology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0175-7598
                1432-0614
                15 June 2020
                15 June 2020
                2020
                : 104
                : 16
                : 6839-6854
                Affiliations
                [1 ]GRID grid.5590.9, ISNI 0000000122931605, Department of Microbiology, , Institute for Water and Wetland Research, Radboud University, ; Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands
                [2 ]GRID grid.5590.9, ISNI 0000000122931605, Soehngen Institute of Anaerobic Microbiology, Radboud University, ; Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands
                Author information
                https://orcid.org/0000-0002-1221-1230
                http://orcid.org/0000-0003-1990-9030
                https://orcid.org/0000-0002-1568-8878
                Article
                10724
                10.1007/s00253-020-10724-7
                7374477
                32542472
                eb72f421-317e-4340-9fc5-3e1767873b58
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 8 April 2020
                : 27 May 2020
                : 4 June 2020
                Funding
                Funded by: Deutsche Forschungsgesellschaft
                Award ID: KU 3768/1-1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: VOLCANO 669371
                Funded by: FundRef http://dx.doi.org/10.13039/501100003246, Nederlandse Organisatie voor Wetenschappelijk Onderzoek;
                Award ID: Gravitation Grant 024.002.002
                Award Recipient :
                Categories
                Mini-Review
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2020

                Biotechnology
                methane production,extended substrate range,novel pathways,archaea
                Biotechnology
                methane production, extended substrate range, novel pathways, archaea

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