Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea

• Published in: Nature communications Vol. 10; no. 1; pp. 4574 - 11
• Main Authors: Hua, Zheng-Shuang, Wang, Yu-Lin, Evans, Paul N., Qu, Yan-Ni, Goh, Kian Mau, Rao, Yang-Zhi, Qi, Yan-Ling, Li, Yu-Xian, Huang, Min-Jun, Jiao, Jian-Yu, Chen, Ya-Ting, Mao, Yan-Ping, Shu, Wen-Sheng, Hozzein, Wael, Hedlund, Brian P., Tyson, Gene W., Zhang, Tong, Li, Wen-Jun
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 08.10.2019; Nature Publishing Group; Nature Portfolio
• Subjects: 45; 49/22; 631/158/855; 631/181/735; 631/208/325/1996; 631/326/26; Alkanes; Alkanes - metabolism; Ammonia; Archaea; Archaea - enzymology; Archaea - genetics; Archaea - isolation & purification; Biodiversity; Biological Evolution; China; Coenzyme M; Computational Biology; Evolutionary genetics; Gene transfer; Genes; Genome, Archaeal; Genomes; High temperature; Hot springs; Hot Springs - microbiology; Hot Temperature; Humanities and Social Sciences; Metabolic Networks and Pathways - genetics; Metabolism; Metagenome; Methane; Methane - metabolism; Methanogenesis; Methanogenic bacteria; Methanotrophic bacteria; Microorganisms; multidisciplinary; Multigene Family - genetics; Oxidation; Oxidoreductases - genetics; Oxidoreductases - metabolism; Phylogeny; Reductase; Reductases; Science; Science (multidisciplinary); China
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-019-12574-y

Several recent studies have shown the presence of genes for the key enzyme associated with archaeal methane/alkane metabolism, methyl-coenzyme M reductase (Mcr), in metagenome-assembled genomes (MAGs) divergent to existing archaeal lineages. Here, we study the mcr -containing archaeal MAGs from several hot springs, which reveal further expansion in the diversity of archaeal organisms performing methane/alkane metabolism. Significantly, an MAG basal to organisms from the phylum Thaumarchaeota that contains mcr genes, but not those for ammonia oxidation or aerobic metabolism, is identified. Together, our phylogenetic analyses and ancestral state reconstructions suggest a mostly vertical evolution of mcrABG genes among methanogens and methanotrophs, along with frequent horizontal gene transfer of mcr genes between alkanotrophs. Analysis of all mcr -containing archaeal MAGs/genomes suggests a hydrothermal origin for these microorganisms based on optimal growth temperature predictions. These results also suggest methane/alkane oxidation or methanogenesis at high temperature likely existed in a common archaeal ancestor. Methane metabolism by some lineages of Archaea contributes to the cycling of carbon on Earth. Here, the authors show high diversity of methyl-coenzyme M reductase (Mcr), a key enzyme associated with archaeal methane/alkane metabolism, in hot spring Archaea, and investigate their ecological roles and evolution.