TY - JOUR
T1 - Evidence for non-methanogenic metabolisms in globally distributed archaeal clades basal to the Methanomassiliicoccales
AU - Zinke, Laura A.
AU - Evans, Paul N.
AU - Santos-Medellín, Christian
AU - Schroeder, Alena L.
AU - Parks, Donovan H.
AU - Varner, Ruth K.
AU - Rich, Virginia I.
AU - Tyson, Gene W.
AU - Emerson, Joanne B.
N1 - Funding Information:
The authors thank Elaina Graham and Lily Momper for advice on phylogenetic tree construction and members of the NSF funded Northern Ecosystems Research for Undergraduates REU Site (EAR#1063037) team, Kaitlyn Steele, Martin Wik, and Nancy Freitas, for sample collection. The support and resources from the High‐Performance Computing group in the Bioinformatics Core at the University of California, Davis are gratefully acknowledged. Our funding sources include new laboratory start‐up to J.B.E. from the UC Davis College of Agricultural and Environmental Sciences and the UC Davis Department of Plant Pathology, and SAL16 MAG recovery via support from the Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research, grants DE‐SC0010580 and DE‐SC0016440 to V.I.R. and G.W.T. Support for C.S.M. was provided by an award from the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program, grant DE‐SC0020163 to J.B.E.
Funding Information:
The authors thank Elaina Graham and Lily Momper for advice on phylogenetic tree construction and members of the NSF funded Northern Ecosystems Research for Undergraduates REU Site (EAR#1063037) team, Kaitlyn Steele, Martin Wik, and Nancy Freitas, for sample collection. The support and resources from the High-Performance Computing group in the Bioinformatics Core at the University of California, Davis are gratefully acknowledged. Our funding sources include new laboratory start-up to J.B.E. from the UC Davis College of Agricultural and Environmental Sciences and the UC Davis Department of Plant Pathology, and SAL16 MAG recovery via support from the Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research, grants DE-SC0010580 and DE-SC0016440 to V.I.R. and G.W.T. Support for C.S.M. was provided by an award from the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program, grant DE-SC0020163 to J.B.E.
Publisher Copyright:
© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.
PY - 2021/1
Y1 - 2021/1
N2 - Recent discoveries of mcr and mcr-like genes in genomes from diverse archaeal lineages suggest that methane metabolism is an ancient pathway with a complicated evolutionary history. One conventional view is that methanogenesis is an ancestral metabolism of the class Thermoplasmata. Through comparative genomic analysis of 12 Thermoplasmata metagenome-assembled genomes (MAGs) basal to the Methanomassiliicoccales, we show that these microorganisms do not encode the genes required for methanogenesis. Further analysis of 770 Ca. Thermoplasmatota genomes/MAGs found no evidence of mcrA homologues outside of the Methanomassiliicoccales. Together, these results suggest that methanogenesis was laterally acquired by an ancestor of the Methanomassiliicoccales. The 12 analysed MAGs include representatives from four orders basal to the Methanomassiliicoccales, including a high-quality MAG that likely represents a new order, Ca. Lunaplasma lacustris ord. nov. sp. nov. These MAGs are predicted to use diverse energy conservation pathways, including heterotrophy, sulfur and hydrogen metabolism, denitrification, and fermentation. Two lineages are widespread among anoxic, sedimentary environments, whereas Ca. Lunaplasma lacustris has thus far only been detected in alpine caves and subarctic lake sediments. These findings advance our understanding of the metabolic potential, ecology, and global distribution of the Thermoplasmata and provide insight into the evolutionary history of methanogenesis within the Ca. Thermoplasmatota.
AB - Recent discoveries of mcr and mcr-like genes in genomes from diverse archaeal lineages suggest that methane metabolism is an ancient pathway with a complicated evolutionary history. One conventional view is that methanogenesis is an ancestral metabolism of the class Thermoplasmata. Through comparative genomic analysis of 12 Thermoplasmata metagenome-assembled genomes (MAGs) basal to the Methanomassiliicoccales, we show that these microorganisms do not encode the genes required for methanogenesis. Further analysis of 770 Ca. Thermoplasmatota genomes/MAGs found no evidence of mcrA homologues outside of the Methanomassiliicoccales. Together, these results suggest that methanogenesis was laterally acquired by an ancestor of the Methanomassiliicoccales. The 12 analysed MAGs include representatives from four orders basal to the Methanomassiliicoccales, including a high-quality MAG that likely represents a new order, Ca. Lunaplasma lacustris ord. nov. sp. nov. These MAGs are predicted to use diverse energy conservation pathways, including heterotrophy, sulfur and hydrogen metabolism, denitrification, and fermentation. Two lineages are widespread among anoxic, sedimentary environments, whereas Ca. Lunaplasma lacustris has thus far only been detected in alpine caves and subarctic lake sediments. These findings advance our understanding of the metabolic potential, ecology, and global distribution of the Thermoplasmata and provide insight into the evolutionary history of methanogenesis within the Ca. Thermoplasmatota.
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U2 - 10.1111/1462-2920.15316
DO - 10.1111/1462-2920.15316
M3 - Article
C2 - 33185945
AN - SCOPUS:85096831998
SN - 1462-2912
VL - 23
SP - 340
EP - 357
JO - Environmental Microbiology
JF - Environmental Microbiology
IS - 1
ER -