4.6 Article

Evidence for non-methanogenic metabolisms in globally distributed archaeal clades basal to the Methanomassiliicoccales

Journal

ENVIRONMENTAL MICROBIOLOGY
Volume 23, Issue 1, Pages -

Publisher

WILEY
DOI: 10.1111/1462-2920.15316

Keywords

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Categories

Funding

  1. NSF [1063037]
  2. High-Performance Computing group in the Bioinformatics Core at the University of California, Davis
  3. UC Davis College of Agricultural and Environmental Sciences
  4. UC Davis Department of Plant Pathology
  5. Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research [DE-SC0010580, DE-SC0016440]
  6. U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program [DE-SC0020163]
  7. U.S. Department of Energy (DOE) [DE-SC0020163] Funding Source: U.S. Department of Energy (DOE)
  8. Division Of Earth Sciences
  9. Directorate For Geosciences [1063037] Funding Source: National Science Foundation

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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. Analysis showed that methanogenesis may have been laterally acquired by an ancestor of the Methanomassiliicoccales. Furthermore, no evidence of mcrA homologues outside of Methanomassiliicoccales was found in Thermoplasmata genomes.
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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