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Title: Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens

Abstract

Methanogenic archaea are major contributors to the global carbon cycle and were long thought to belong exclusively to the euryarchaeal phylum. Discovery of the methanogenesis gene cluster methyl-coenzyme M reductase (Mcr) in the Bathyarchaeota, and thereafter the Verstraetearchaeota, led to a paradigm shift, pushing back the evolutionary origin of methanogenesis to predate that of the Euryarchaeota. The methylotrophic methanogenesis found in the non-Euryarchaota distinguished itself from the predominantly hydrogenotrophic methanogens found in euryarchaeal orders as the former do not couple methanogenesis to carbon fixation through the reductive acetyl-CoA [Wood–Ljungdahl pathway (WLP)], which was interpreted as evidence for independent evolution of the two methanogenesis pathways. Here, we report the discovery of a complete and divergent hydrogenotrophic methanogenesis pathway in a thermophilic order of the Verstraetearchaeota, which we have named Candidatus Methanohydrogenales, as well as the presence of the WLP in the crenarchaeal order Desulfurococcales. Our findings support the ancient origin of hydrogenotrophic methanogenesis, suggest that methylotrophic methanogenesis might be a later adaptation of specific orders, and provide insight into how the transition from hydrogenotrophic to methylotrophic methanogenesis might have occurred.

Authors:
ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1497216
Alternate Identifier(s):
OSTI ID: 1581744
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 11; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; methanogenesis; archaea; evolution

Citation Formats

Berghuis, Bojk A., Yu, Feiqiao Brian, Schulz, Frederik, Blainey, Paul C., Woyke, Tanja, and Quake, Stephen R. Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens. United States: N. p., 2019. Web. doi:10.1073/pnas.1815631116.
Berghuis, Bojk A., Yu, Feiqiao Brian, Schulz, Frederik, Blainey, Paul C., Woyke, Tanja, & Quake, Stephen R. Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens. United States. doi:https://doi.org/10.1073/pnas.1815631116
Berghuis, Bojk A., Yu, Feiqiao Brian, Schulz, Frederik, Blainey, Paul C., Woyke, Tanja, and Quake, Stephen R. Wed . "Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens". United States. doi:https://doi.org/10.1073/pnas.1815631116.
@article{osti_1497216,
title = {Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens},
author = {Berghuis, Bojk A. and Yu, Feiqiao Brian and Schulz, Frederik and Blainey, Paul C. and Woyke, Tanja and Quake, Stephen R.},
abstractNote = {Methanogenic archaea are major contributors to the global carbon cycle and were long thought to belong exclusively to the euryarchaeal phylum. Discovery of the methanogenesis gene cluster methyl-coenzyme M reductase (Mcr) in the Bathyarchaeota, and thereafter the Verstraetearchaeota, led to a paradigm shift, pushing back the evolutionary origin of methanogenesis to predate that of the Euryarchaeota. The methylotrophic methanogenesis found in the non-Euryarchaota distinguished itself from the predominantly hydrogenotrophic methanogens found in euryarchaeal orders as the former do not couple methanogenesis to carbon fixation through the reductive acetyl-CoA [Wood–Ljungdahl pathway (WLP)], which was interpreted as evidence for independent evolution of the two methanogenesis pathways. Here, we report the discovery of a complete and divergent hydrogenotrophic methanogenesis pathway in a thermophilic order of the Verstraetearchaeota, which we have named Candidatus Methanohydrogenales, as well as the presence of the WLP in the crenarchaeal order Desulfurococcales. Our findings support the ancient origin of hydrogenotrophic methanogenesis, suggest that methylotrophic methanogenesis might be a later adaptation of specific orders, and provide insight into how the transition from hydrogenotrophic to methylotrophic methanogenesis might have occurred.},
doi = {10.1073/pnas.1815631116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 11,
volume = 116,
place = {United States},
year = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: https://doi.org/10.1073/pnas.1815631116

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Cited by: 15 works
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