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

Zheng-Shuang Hua,Wael Hozzein,Wen-Jun Li,Yu-Lin Wang,Yu-Xian Li,Min-Jun Huang,Yan-Ping Mao,Yan-Ling Qi,Paul N Evans,Yan-Ni Qu,Tong Zhang,Gene W Tyson,Yang-Zhi Rao,Ya-Ting Chen,Brian P Hedlund,Jian-Yu Jiao,Kian Mau Goh,Wen-Sheng Shu

doi:10.1038/s41467-019-12574-y

Abstract

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.

Highlights

Together these results show that hot spring environments harbor many mcr-containing organisms from outside of the Euryarchaeota and further expand the diversity of Mcr meditated methane or alkane metabolism processes
We propose a plausible evolutionary scenario where the common ancestor of archaea harbors the ability for methane metabolism that is mostly the result of vertical inheritance, with some HGT events
Frequent HGT events have led to alkanotrophy being found in several lineages that cannot be explained by vertical descent of mcr genes

Summary

Introduction

We infer that these mcr-containing archaea may originate from thermal habitats such as hydrothermal vents or terrestrial hot springs predicted by a high ancestral optimal growth temperature. For functional genes, including concatenated mcrABG genes and individual subunits of these three genes, sequences were aligned using MUSCLE and IQ-tree was used to infer maximum-likelihood phylogenies with the same parameters as above. Amino acid sequences at all internal nodes were computationally inferred based on the sequence alignment and tree topology of concatenated mcrABG gene (as described above) using codelml program in PAML45 package (v4.9 h). The type species is “Ca. Methanohydrogenotrophicum pristinum”. Archeo ancient, referring to Archaea; Methanogeoarchaeum, methane (-producing) terrestrial archaeon. The type species is “Ca. Methanogeoarchaeum hydrogenovorans”.

Results

Conclusion