Genomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>

ABSTRACT 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) retriev...

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Autores principales: Yi-Fan Liu, Jing Chen, Livia S. Zaramela, Li-Ying Wang, Serge Maurice Mbadinga, Zhao-Wei Hou, Xiao-Lin Wu, Ji-Dong Gu, Karsten Zengler, Bo-Zhong Mu
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Publicado: American Society for Microbiology 2020
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HGT
Acceso en línea:https://doaj.org/article/9e91808439d24706948115d91a8eefe0
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spelling oai:doaj.org-article:9e91808439d24706948115d91a8eefe02021-12-02T19:46:20ZGenomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>10.1128/mSystems.00651-192379-5077https://doaj.org/article/9e91808439d24706948115d91a8eefe02020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00651-19https://doaj.org/toc/2379-5077ABSTRACT 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.Yi-Fan LiuJing ChenLivia S. ZaramelaLi-Ying WangSerge Maurice MbadingaZhao-Wei HouXiao-Lin WuJi-Dong GuKarsten ZenglerBo-Zhong MuAmerican Society for Microbiologyarticlehorizontal gene transferHGTmetatranscriptomicsmethyl-coenzyme M reductase complexMCR complexoil reservoirMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution DOAJ
collection DOAJ
language EN
topic horizontal gene transfer
HGT
metatranscriptomics
methyl-coenzyme M reductase complex
MCR complex
oil reservoir
Microbiology
QR1-502
spellingShingle horizontal gene transfer
HGT
metatranscriptomics
methyl-coenzyme M reductase complex
MCR complex
oil reservoir
Microbiology
QR1-502
Yi-Fan Liu
Jing Chen
Livia S. Zaramela
Li-Ying Wang
Serge Maurice Mbadinga
Zhao-Wei Hou
Xiao-Lin Wu
Ji-Dong Gu
Karsten Zengler
Bo-Zhong Mu
Genomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>
description ABSTRACT 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.
format article
author Yi-Fan Liu
Jing Chen
Livia S. Zaramela
Li-Ying Wang
Serge Maurice Mbadinga
Zhao-Wei Hou
Xiao-Lin Wu
Ji-Dong Gu
Karsten Zengler
Bo-Zhong Mu
author_facet Yi-Fan Liu
Jing Chen
Livia S. Zaramela
Li-Ying Wang
Serge Maurice Mbadinga
Zhao-Wei Hou
Xiao-Lin Wu
Ji-Dong Gu
Karsten Zengler
Bo-Zhong Mu
author_sort Yi-Fan Liu
title Genomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>
title_short Genomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>
title_full Genomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>
title_fullStr Genomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>
title_full_unstemmed Genomic and Transcriptomic Evidence Supports Methane Metabolism in <italic toggle="yes">Archaeoglobi</italic>
title_sort genomic and transcriptomic evidence supports methane metabolism in <italic toggle="yes">archaeoglobi</italic>
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/9e91808439d24706948115d91a8eefe0
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