Genomic and transcriptomic evidence supports methane metabolism in Archaeoglobi

TY - JOUR

T1 - Genomic and transcriptomic evidence supports methane metabolism in Archaeoglobi

AU - Liu, Yi Fan

AU - Chen, Jing

AU - Zaramela, Livia S.

AU - Wang, Li Ying

AU - Mbadinga, Serge Maurice

AU - Hou, Zhao Wei

AU - Wu, Xiao Lin

AU - Gu, Ji Dong

AU - Zengler, Karsten

AU - Mu, Bo Zhong

N1 - Publisher Copyright: Copyright © 2020 Liu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

PY - 2020

Y1 - 2020

N2 - Euryarchaeal lineages have been believed to have a methanogenic last common ancestor. However, members of euryarchaeal Archaeoglobi have long been considered nonmethanogenic and their evolutionary history remains elusive. Here, three high-quality metagenomic-assembled genomes (MAGs) retrieved from high-temperature oil reservoir and hot springs, together with three newly assembled Archaeoglobi MAGs from previously reported hot spring metagenomes, are demonstrated to represent a novel genus of Archaeoglobaceae, “Candidatus Methanomixophus.” All “Ca. Methanomixophus” MAGs encode an M methyltransferase (MTR) complex and a traditional type of methyl-coenzyme M reductase (MCR) complex, which is different from the divergent MCR complexes found in “Ca. Polytropus marinifundus.” In addition, “Ca. Methanomixophus dualitatem” MAGs preserve the genomic capacity for dissimilatory sulfate reduction. Comparative phylogenetic analysis supports a laterally transferred origin for an MCR complex and vertical heritage of the MTR complex in this lineage. Metatranscriptomic analysis revealed concomitant in situ activity of hydrogen-dependent methylotrophic methanogenesis and heterotrophic fermentation within populations of “Ca. Methanomixophus hydrogenotrophicum” in a high-temperature oil reservoir. IMPORTANCE Current understanding of the diversity, biology, and ecology of Archaea is very limited, especially considering how few of the known phyla have been cultured or genomically explored. The reconstruction of “Ca. Methanomixophus” MAGs not only expands the known range of metabolic versatility of the members of Archaeoglobi but also suggests that the phylogenetic distribution of MCR and MTR complexes is even wider than previously anticipated.

AB - Euryarchaeal lineages have been believed to have a methanogenic last common ancestor. However, members of euryarchaeal Archaeoglobi have long been considered nonmethanogenic and their evolutionary history remains elusive. Here, three high-quality metagenomic-assembled genomes (MAGs) retrieved from high-temperature oil reservoir and hot springs, together with three newly assembled Archaeoglobi MAGs from previously reported hot spring metagenomes, are demonstrated to represent a novel genus of Archaeoglobaceae, “Candidatus Methanomixophus.” All “Ca. Methanomixophus” MAGs encode an M methyltransferase (MTR) complex and a traditional type of methyl-coenzyme M reductase (MCR) complex, which is different from the divergent MCR complexes found in “Ca. Polytropus marinifundus.” In addition, “Ca. Methanomixophus dualitatem” MAGs preserve the genomic capacity for dissimilatory sulfate reduction. Comparative phylogenetic analysis supports a laterally transferred origin for an MCR complex and vertical heritage of the MTR complex in this lineage. Metatranscriptomic analysis revealed concomitant in situ activity of hydrogen-dependent methylotrophic methanogenesis and heterotrophic fermentation within populations of “Ca. Methanomixophus hydrogenotrophicum” in a high-temperature oil reservoir. IMPORTANCE Current understanding of the diversity, biology, and ecology of Archaea is very limited, especially considering how few of the known phyla have been cultured or genomically explored. The reconstruction of “Ca. Methanomixophus” MAGs not only expands the known range of metabolic versatility of the members of Archaeoglobi but also suggests that the phylogenetic distribution of MCR and MTR complexes is even wider than previously anticipated.

KW - HGT

KW - Horizontal gene transfer

KW - MCR complex

KW - Metatranscriptomics

KW - Methanogens

KW - Methyl-coenzyme M reductase complex

KW - Oil reservoir

UR - http://www.scopus.com/inward/record.url?scp=85082000837&partnerID=8YFLogxK

U2 - 10.1128/mSystems.00651-19

DO - 10.1128/mSystems.00651-19

M3 - 文章

AN - SCOPUS:85082000837

SN - 2379-5077

VL - 5

JO - mSystems

JF - mSystems

IS - 2

M1 - e00651-19

ER -