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:

Berghuis, Bojk A. ;

• Search DOE PAGES for author "Berghuis, Bojk A."
• Search DOE PAGES for ORCID "0000-0002-7797-0553"

Yu, Feiqiao Brian ;

• Search DOE PAGES for author "Yu, Feiqiao Brian"
• Search DOE PAGES for ORCID "0000-0003-3416-3046"

Schulz, Frederik ;

• Search DOE PAGES for author "Schulz, Frederik"
• Search DOE PAGES for ORCID "0000-0002-4932-4677"

Blainey, Paul C. ;

• Search DOE PAGES for author "Blainey, Paul C."
• Search DOE PAGES for ORCID "0000-0002-4889-8783"

Woyke, Tanja ;

• Search DOE PAGES for author "Woyke, Tanja"
• Search DOE PAGES for ORCID "0000-0002-9485-5637"

Quake, Stephen R.

• Search DOE PAGES for author "Quake, Stephen R."
• Search DOE PAGES for ORCID "0000-0002-1613-0809"

Publication Date:

Wed Feb 27 00:00:00 EST 2019

Research Org.:

Lawrence Berkeley National Laboratory (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