Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine

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dc.contributor.author Borrel, Guillaume
dc.contributor.author Parisot, Nicolas
dc.contributor.author Harris, Hugh Michael B.
dc.contributor.author Peyretaillade, Eric
dc.contributor.author Gaci, Nadia
dc.contributor.author Tottey, William
dc.contributor.author Bardot, Olivier
dc.contributor.author Raymann, Kasie
dc.contributor.author Gribaldo, Simonetta
dc.contributor.author Peyret, Pierre
dc.contributor.author O'Toole, Paul W.
dc.contributor.author Brugère, Jean-François
dc.date.accessioned 2016-01-25T15:20:45Z
dc.date.available 2016-01-25T15:20:45Z
dc.date.issued 2014-08-13
dc.identifier.citation BORREL, G., PARISOT, N., HARRIS, H. M., PEYRETAILLADE, E., GACI, N., TOTTEY, W., BARDOT, O., RAYMANN, K., GRIBALDO, S., PEYRET, P., O’TOOLE, P. W. & BRUGÈRE, J.-F. 2014. Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics, 15:679, 1-24. http://dx.doi.org/10.1186/1471-2164-15-679 en
dc.identifier.volume 15 en
dc.identifier.startpage 1 en
dc.identifier.endpage 24 en
dc.identifier.issn 1471-2164
dc.identifier.uri http://hdl.handle.net/10468/2211
dc.identifier.doi 10.1186/1471-2164-15-679
dc.description.abstract BACKGROUND: A seventh order of methanogens, the Methanomassiliicoccales, has been identified in diverse anaerobic environments including the gastrointestinal tracts (GIT) of humans and other animals and may contribute significantly to methane emission and global warming. Methanomassiliicoccales are phylogenetically distant from all other orders of methanogens and belong to a large evolutionary branch composed by lineages of non-methanogenic archaea such as Thermoplasmatales, the Deep Hydrothermal Vent Euryarchaeota-2 (DHVE-2, Aciduliprofundum boonei) and the Marine Group-II (MG-II). To better understand this new order and its relationship to other archaea, we manually curated and extensively compared the genome sequences of three Methanomassiliicoccales representatives derived from human GIT microbiota, “Candidatus Methanomethylophilus alvus", “Candidatus Methanomassiliicoccus intestinalis” and Methanomassiliicoccus luminyensis. RESULTS: Comparative analyses revealed atypical features, such as the scattering of the ribosomal RNA genes in the genome and the absence of eukaryotic-like histone gene otherwise present in most of Euryarchaeota genomes. Previously identified in Thermoplasmatales genomes, these features are presently extended to several completely sequenced genomes of this large evolutionary branch, including MG-II and DHVE2. The three Methanomassiliicoccales genomes share a unique composition of genes involved in energy conservation suggesting an original combination of two main energy conservation processes previously described in other methanogens. They also display substantial differences with each other, such as their codon usage, the nature and origin of their CRISPRs systems and the genes possibly involved in particular environmental adaptations. The genome of M. luminyensis encodes several features to thrive in soil and sediment conditions suggesting its larger environmental distribution than GIT. Conversely, “Ca. M. alvus” and “Ca. M. intestinalis” do not present these features and could be more restricted and specialized on GIT. Prediction of the amber codon usage, either as a termination signal of translation or coding for pyrrolysine revealed contrasted patterns among the three genomes and suggests a different handling of the Pyl-encoding capacity. CONCLUSIONS: This study represents the first insights into the genomic organization and metabolic traits of the seventh order of methanogens. It suggests contrasted evolutionary history among the three analyzed Methanomassiliicoccales representatives and provides information on conserved characteristics among the overall methanogens and among Thermoplasmata en
dc.description.sponsorship Science Foundation Ireland (Principal Investigator award, CSET award); Department of Agriculture, Food and the Marine, Ireland (FHRI award); European Union (PhD Scholarship Support); Direction Generale de l'Armement, France (PhD Scholarship support); Ministere de l'Enseignement Superieur et de la Recherche, France (PhD Scholarship support); Conseil Régional d'Auvergne, France (Phd Scholarship support); Investissements d'Avenir (grant "Ancestrome" (ANR-10- BINF-01-01)); Paul W. Zuccaire Foundation en
dc.format.mimetype application/pdf en
dc.language.iso en en
dc.publisher Biomed Central Ltd. en
dc.rights © 2014 Borrel et al.; licensee BioMed Central Ltd., 2014. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. en
dc.rights.uri http://creativecommons.org/licenses/by/2.0/ en
dc.subject Archaea en
dc.subject Methanomassiliicoccales en
dc.subject Methanomethylophilus en
dc.subject Origin of replication (ORI) binding (ORB) motif en
dc.subject Genome streamlining en
dc.subject CRISPR en
dc.subject Pyrrolysine Pyl en
dc.subject Energy conservation en
dc.subject Provides acquired-resistance en
dc.subject Short palindromic repeats en
dc.subject Human gut en
dc.subject Methanosarcina-mazei en
dc.subject Transfer-rna en
dc.subject Evolutionary genomics en
dc.subject Ech hydrogenase en
dc.subject Glycine betaine en
dc.subject High-throughput en
dc.title Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine en
dc.type Article (peer-reviewed) en
dc.internal.authorcontactother Guillaume Borrel, Microbiology, University College Cork, Cork, Ireland. +353-21-490-3000 Email: gborrel@ucc.ie en
dc.internal.availability Full text available en
dc.description.version Published Version en
dc.contributor.funder Science Foundation Ireland en
dc.contributor.funder European Commission en
dc.contributor.funder Department of Agriculture, Food and the Marine, Ireland en
dc.contributor.funder Ministère de l'Enseignement Supérieur et de la Recherche, France
dc.contributor.funder Direction Générale de l'Armement, France
dc.contributor.funder Conseil Régional d'Auvergne, France en
dc.contributor.funder Investissements d'Avenir, France
dc.contributor.funder Paul W. Zuccaire Foundation, United States en
dc.description.status Peer reviewed en
dc.identifier.journaltitle BMC Genomics en
dc.internal.copyrightchecked Open Access articles licensed via CC-BY 2.0 with UCC affiliated authors. Uploaded Jan 2016. en
dc.internal.IRISemailaddress gborrel@ucc.ie en
dc.identifier.articleid 679


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© 2014 Borrel et al.; licensee BioMed Central Ltd., 2014. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Except where otherwise noted, this item's license is described as © 2014 Borrel et al.; licensee BioMed Central Ltd., 2014. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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