The genome of Pelotomaculum thermopropionicum reveals niche-associated evolution in anaerobic microbiota

Abstract

The anaerobic biodegradation of organic matter is accomplished by sequential syntrophic catabolism by microbes in different niches. Pelotomaculum thermopropionicum is a representative syntrophic bacterium that catalyzes the intermediate bottleneck step in the anaerobic-biodegradation process, whereby volatile fatty acids (VFAs) and alcohols produced by upstream fermenting bacteria are converted to acetate, hydrogen, and carbon dioxide (substrates for downstream methanogenic archaea). To reveal genomic features that contribute to our understanding of the ecological niche and evolution of P. thermopropionicum, we sequenced its 3,025,375-bp genome and performed comparative analyses with genomes of other community members available in the databases. In the genome, 2920 coding sequences (CDSs) were identified. These CDSs showed a distinct distribution pattern in the functional categories of the Clusters of Orthologous Groups database, which is considered to reflect the niche of this organism. P. thermopropionicum has simple catabolic pathways, in which the propionate-oxidizing methylmalonyl-CoA pathway constitutes the backbone and is linked to several peripheral pathways. Genes for most of the important catabolic enzymes are physically linked to those for PAS-domain-containing regulators, suggesting that the catabolic pathways are regulated in response to environmental conditions and/or global cellular situations rather than specific substrates. Comparative analyses of codon usages revealed close evolutionary relationships between P. thermopropionicum and other niche members, while it was distant from phylogenetically related sugar-fermenting bacteria. These analyses suggest that P. thermopropionicum has evolved as a syntrophy specialist by interacting with niche-associated microbes.

Inter-phylum HGT has shaped the metabolism of many mesophilic and anaerobic bacteria

“…These results were consistent with previous phylogenetic approaches that showed high gene sharing between syntrophic organisms (Cordero and Hogeweg, 2009). Additionally, it has been suggested that HGT is responsible for similar codon usage bias between Pelotomaculum thermopropionicum and other syntrophic organisms (Kosaka et al, 2008) and that syntrophic interactions between Desulfovibrio vulgaris and Methanosarcina barkeri had evolved as a result of ancestral HGT (Scholten et al, 2007). In conclusion, the previous syntrophic organisms represent examples of how tight ecological relationships (that is, physiological dependence and physical contact) have favored the transfer of genetic material between distantly related organisms.…”

Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii , studied in twins

“…YIT12065, is only 82-92% identical to these co-occurring OTUs; very little is known about this isolate's biology. The presence of obligate syntrophs for methanogens in the human gut would not be surprising, because they are known to exist in other environments, such as sludge (39,40).…”

Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor

“…Cloacimonetes': syntrophic propionate degraders This ecogenomic effort also generated a pangenome for Atribacteria, another poorly characterized candidate phylum associated with methanogenic environments ) that our previous study could not address. This Atribacteria encodes propionate metabolism and specifically expresses methylmalonyl-CoA pathway genes with high homology (52-71%) to those found in Pelotomaculum thermopropionicum strain SI, a representative thermophilic propionate-degrading syntroph (Supplementary Table S11; Kosaka et al, 2008). For energy-conserving electron disposal, Atribacteria expresses an electron-bifurcating formate dehydrogenase (Wang et al, 2013) and Fd red -dependent energy-conserving membranebound hydrogenase (Figures 2 and 3), suggesting that both formate and H 2 generation may take part in propionate degradation as observed in Syntrophobacter (Harmsen et al, 1998).…”