Methanogenic archaea are known as human gut inhabitants since more than 30 years ago through the detection of methane in the breath and isolation of two methanogenic species belonging to the order Methanobacteriales, Methanobrevibacter smithii and Methanosphaera stadtmanae. During the last decade, diversity of archaea encountered in the human gastrointestinal tract (GIT) has been extended by sequence identification and culturing of new strains. Here we provide an updated census of the archaeal diversity associated with the human GIT and their possible role in the gut physiology and health. We particularly focus on the still poorly characterized 7th order of methanogens, the Methanomassiliicoccales, associated to aged population. While also largely distributed in non-GIT environments, our actual knowledge on this novel order of methanogens has been mainly revealed through GIT inhabitants. They enlarge the number of final electron acceptors of the gut metabolites to mono- di- and trimethylamine. Trimethylamine is exclusively a microbiota-derived product of nutrients (lecithin, choline, TMAO, L-carnitine) from normal diet, from which seems originate two diseases, trimethylaminuria (or Fish-Odor Syndrome) and cardiovascular disease through the proatherogenic property of its oxidized liver-derived form. This therefore supports interest on these methanogenic species and its use as archaebiotics, a term coined from the notion of archaea-derived probiotics.
BackgroundA 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.ResultsComparative 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.ConclusionsThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-679) contains supplementary material, which is available to authorized users.
We report the draft genome sequence of "Candidatus Methanomethylophilus alvus" Mx1201, a methanogen present in the human gut. It was enriched from human feces under anaerobic conditions with methanol as the substrate. Its circular genome, of around 1.7 Mb, contains genes needed for methylotrophic methanogenesis from methanol and tri-, di-, and monomethylamine. Methanogenic archaea play a crucial role in the functioning of digestive ecosystems through the consumption of the hydrogen generated during anaerobic fermentations (3). The first archaeal species associated to the human gut, Methanobrevibacter smithii and Methanosphaera stadtmanae (order Methanobacteriales), were cultured and described 30 years ago (12, 13). During the last decade, the diversity of the human-associated archaea was progressively enlarged by the detection of 16S rRNA genes affiliated to the Crenarchaeota (15), to the Halobacteriales (14), and to a Thermoplasmatales-related lineage (10,11,16). A species of the latter lineage, Methanomassiliicoccus luminyensis, was recently isolated and described as a methanogen growing on methanol and hydrogen only (5). More recently, its genome was sequenced (6).To allow genomic characterization of novel methanogens, we performed enrichment cultures targeting methanogens in feces of elderly people (68 to 93 years old), selecting for the presence of a Thermoplasmatales-related lineage. Enrichment cultures carried out with methanol as the substrate led to the progressive dominance of "Candidatus Methanomethylophilus alvus" over the microbial community. This archaeon is distantly related to its closest related species, M. luminyensis and Aciduliprofundum boonei, with 87% and 80% 16S rRNA gene sequence identity, respectively. Sequences of 16S rRNA genes of uncultured archaea with more than 97% identity to "Ca. Methanomethylophilus alvus" have previously been recurrently retrieved in the digestive tract of various animals, suggesting that these archaea are specifically associated to these environments. Those sequences form a portion of the previously described rumen cluster C (8).A 3-kb mate-paired library was constructed and sequenced from a quarter plate of a 454 GS FLX Titanium run (Macrogen, Republic of Korea). A total of 347,052 reads corresponding to 158 Mb were obtained. The reads were assembled with a GS De Novo assembler (version 2.6), first in 15 contigs (average depth coverage of 36.9-fold) and then in a unique scaffold of 1,664,410 bp. The gaps between the contigs were partially closed using GapFiller (2) and by sequencing of PCR products (4 remaining gaps). Around 1,800 bp was lacking between the two scaffold termini, as shown by PCR amplification. The open reading frames were predicted with Glimmer 3 (4) and annotated using RAST (1).The genome of "Ca. Methanomethylophilus alvus" has a GϩC content of 55.6%, 44 usual tRNA genes, a single copy of each of the 23S and 16S rRNA genes, and 2 noncontiguous copies of 5S rRNA genes that were distant in the genome from the 23S and 16S rRNA genes. A total of 1...
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