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.authorBorrel, Guillaume
dc.contributor.authorParisot, Nicolas
dc.contributor.authorHarris, Hugh Michael B.
dc.contributor.authorPeyretaillade, Eric
dc.contributor.authorGaci, Nadia
dc.contributor.authorTottey, William
dc.contributor.authorBardot, Olivier
dc.contributor.authorRaymann, Kasie
dc.contributor.authorGribaldo, Simonetta
dc.contributor.authorPeyret, Pierre
dc.contributor.authorO'Toole, Paul W.
dc.contributor.authorBrugère, Jean-François
dc.contributor.funderScience Foundation Irelanden
dc.contributor.funderEuropean Commissionen
dc.contributor.funderDepartment of Agriculture, Food and the Marine, Irelanden
dc.contributor.funderMinistère de l'Enseignement Supérieur et de la Recherche, France
dc.contributor.funderDirection Générale de l'Armement, France
dc.contributor.funderConseil Régional d'Auvergne, Franceen
dc.contributor.funderInvestissements d'Avenir, France
dc.contributor.funderPaul W. Zuccaire Foundation, United Statesen
dc.date.accessioned2016-01-25T15:20:45Z
dc.date.available2016-01-25T15:20:45Z
dc.date.issued2014-08-13
dc.description.abstractBACKGROUND: 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 Thermoplasmataen
dc.description.sponsorshipScience 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 Foundationen
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.articleid679
dc.identifier.citationBORREL, 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/10.1186/1471-2164-15-679en
dc.identifier.doi10.1186/1471-2164-15-679
dc.identifier.endpage24en
dc.identifier.issn1471-2164
dc.identifier.journaltitleBMC Genomicsen
dc.identifier.startpage1en
dc.identifier.urihttps://hdl.handle.net/10468/2211
dc.identifier.volume15en
dc.language.isoenen
dc.publisherBiomed 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.urihttp://creativecommons.org/licenses/by/2.0/en
dc.subjectArchaeaen
dc.subjectMethanomassiliicoccalesen
dc.subjectMethanomethylophilusen
dc.subjectOrigin of replication (ORI) binding (ORB) motifen
dc.subjectGenome streamliningen
dc.subjectCRISPRen
dc.subjectPyrrolysine Pylen
dc.subjectEnergy conservationen
dc.subjectProvides acquired-resistanceen
dc.subjectShort palindromic repeatsen
dc.subjectHuman guten
dc.subjectMethanosarcina-mazeien
dc.subjectTransfer-rnaen
dc.subjectEvolutionary genomicsen
dc.subjectEch hydrogenaseen
dc.subjectGlycine betaineen
dc.subjectHigh-throughputen
dc.titleComparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysineen
dc.typeArticle (peer-reviewed)en
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