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In this opinion article, I wish to highlight the fact that reactions linked to tetrahydromethanopterin (H4MPT) and methanofuran (MF), the ones involved in methanogenesis as well as in methylotrophy, are much more widespread among both Bacteria and Archaea than originally thought. While, over the past two decades, databases of the respective genes have been steadily growing and expanding to include novel, divergent sequences, belonging to a variety of taxa, somehow a view still prevails of the limited distribution of these genes, along with an evolutionary scenario in which genes for the methanogenesis pathway were horizontally transferred from Euryarchaea into Proteobacteria (Graham et al., 2000; Gogarten et al., 2002; Boucher et al., 2003; Braakman and Smith, 2012; Arnold, 2015). The two main arguments originally used to support this scenario were (1) the limited distribution of the H4MPT/MF-dependent pathway in the bacterial domain of life, and (2) the low probability of the respective genes being lost in most bacterial lineages (Boucher et al., 2003). However, these arguments can be easily refuted in the light of the current knowledge. In Figure ​Figure1,1, I utilize the recently constructed universal tree of life (Hug et al., 2016), to map the taxa in which at least some of the genes for the H4MPT/MF-dependent C1 transfers are recognized. Among the Archaea, these include, in addition to the well-characterized methanonogens or methane oxidizers, members of Euryarchaeota not known for a methanogenic life style (Thermoplasmatales, Hadesarchaea; Baker et al., 2016), members of Crenarchaeota (Thermoproteales, Ignisphaera, Ingnispaeroid; Goker et al., 2010; Jay et al., 2016), Bathyarchaeota (Evans et al., 2015; Lazar et al., 2016), and Thorarchaeota (Seitz et al., 2016). Among the Bacteria, genes for the H4MPT/MF-dependent reactions have been identified, beside Alpha-, Beta-, and Gammaproteobacteria (Vorholt et al., 1999), in the genomes of Planctomycetes (Chistoserdova et al., 2004; Chistoserdova, 2013), Deltaproteobacteria, Firmicutes, Actinomycetes, Synergistetes, Chloroflexi (Brown et al., 2011 and unpublished genomes available through the NCBI), as well as in the Candidate phylum NC10 (Ettwig et al., 2010). This wide distribution across the tree of life (Figure ​(Figure1),1), along with great sequence divergence for the genes in question (Chistoserdova, 2013; Evans et al., 2015; Spang et al., 2015) support a scenario of a long evolution within both Archaea and Bacteria, and point to the emergence of these reactions in early life, before Bacteria and Archaea have branched apart.

Methanogenesis and methane oxidation are the major biological processes affecting the global cycling of the powerful greenhouse gas methane. To carry out the two alternative bioconversions, Nature has cleverly recycled key reactions for the C-1 transfers between the oxidation levels of formaldehyde and formate, and these involve analogous enzyme systems and common specialized cofactors, methanopterin and methanofuran. Until recently, the distribution of these functions has been limited to methanogenic archaea and methylotrophic proteobacteria, and their evolutionary history remained obscure. Single interdomain lateral transfer of the respective genes has been suggested to play a role. Here we show that genes for C-1 transfer reactions linked to methanopterin and methanofuran are also present in diverse representatives of the enigmatic bacterial clade, the Planctomycetes. Phylogenetic analysis places the planctomycete sequences as distantly from their archaeal counterparts as from their proteobacterial counterparts, suggesting novel scenarios for the evolution of the C-1 transfer functions in both methanogens and methylotrophs. This finding suggests a possible role for Planctomycetes in the evolution of the methane cycle on Earth., Organismic and Evolutionary Biology