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Title: Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota

Journal Article · · Nature Microbiology
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6];  [6];  [7]; ORCiD logo [8]
  1. Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences; Montana State Univ., Bozeman, MT (United States). Center for Biofilm Engineering
  2. Montana State Univ., Bozeman, MT (United States). Dept. of Microbiology and Immunology
  3. Montana State Univ., Bozeman, MT (United States). Center for Biofilm Engineering; Montana State Univ., Bozeman, MT (United States). Dept. of Microbiology and Immunology
  4. Univ. of Chicago, IL (United States). Dept. of Medicine
  5. Univ. of Chicago, IL (United States). Dept. of Medicine; Marine Biological Laboratory, Woods Hole, MA (United States). Josephine Bay Paul Center
  6. Montana State Univ., Bozeman, MT (United States). Center for Biofilm Engineering
  7. Indiana Univ., Bloomington, IN (United States). Informatics Group
  8. Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences; Montana State Univ., Bozeman, MT (United States). Thermal Biology Institute

Phylogenetic and geological evidence supports the hypothesis that life on Earth originated in thermal environments and conserved energy through methanogenesis or sulfur reduction. Here we describe two populations of the deeply rooted archaeal phylum Korarchaeota, which were retrieved from the metagenome of a circumneutral, suboxic hot spring that contains high levels of sulfate, sulfide, methane, hydrogen and carbon dioxide. One population is closely related to ‘Candidatus Korarchaeum cryptofilum OPF8’, while the more abundant korarchaeote, ‘Candidatus Methanodesulfokores washburnensis’, contains genes that are necessary for anaerobic methane and dissimilatory sulfur metabolisms. Phylogenetic and ancestral reconstruction analyses suggest that methane metabolism originated in the Korarchaeota, whereas genes for dissimilatory sulfite reduction were horizontally transferred to the Korarchaeota from the Firmicutes. Interactions among enzymes involved in both metabolisms could facilitate exergonic, sulfite-dependent, anaerobic oxidation of methane to methanol; alternatively, ‘Ca. M. washburnensis’ could conduct methanogenesis and sulfur reduction independently. Metabolic reconstruction suggests that ‘Ca. M. washburnensis’ is a mixotroph, capable of amino acid uptake, assimilation of methane-derived carbon and/or CO2 fixation by archaeal type III-b RuBisCO for scavenging ribose carbon. Our findings link anaerobic methane metabolism and dissimilatory sulfur reduction within a single deeply rooted archaeal population and have implications for the evolution of these traits throughout the Archaea.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1779059
Journal Information:
Nature Microbiology, Vol. 4, Issue 4; ISSN 2058-5276
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (73)

A korarchaeal genome reveals insights into the evolution of the Archaea journal June 2008
Anvi’o: an advanced analysis and visualization platform for ‘omics data journal January 2015
Asgard archaea illuminate the origin of eukaryotic cellular complexity journal January 2017
Diversity of Methane-Cycling Archaea in Hydrothermal Sediment Investigated by General and Group-Specific PCR Primers journal December 2014
Domain Evolution and Functional Diversification of Sulfite Reductases journal February 2005
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics journal October 2015
The microbial pan-genome journal December 2005
Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota journal July 2018
Shifting the genomic gold standard for the prokaryotic species definition journal October 2009
In vitro methanol production from methyl coenzyme M using the Methanosarcina barkeri MtaABC protein complex journal June 2017
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea journal August 2017
Using MCL to Extract Clusters from Networks book October 2011
Methane-consuming archaebacteria in marine sediments journal April 1999
Complex Evolution of the Mismatch Repair System in Eukaryotes is Illuminated by Novel Archaeal Genomes journal January 2021
Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces journal August 2012
Isotopic evidence for microbial sulphate reduction in the early Archaean era journal March 2001
New Mode of Energy Metabolism in the Seventh Order of Methanogens as Revealed by Comparative Genome Analysis of “Candidatus Methanoplasma termitum” journal December 2014
Archaeal Type III RuBisCOs Function in a Pathway for AMP Metabolism journal February 2007
Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era journal March 2006
Community-wide analysis of microbial genome sequence signatures journal January 2009
Mutagenesis of the C1 Oxidation Pathway in Methanosarcina barkeri: New Insights into the Mtr/Mer Bypass Pathway journal January 2008
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens journal April 2002
Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life journal August 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Single cell activity reveals direct electron transfer in methanotrophic consortia journal September 2015
Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes journal February 2009
Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats journal May 2018
The COG database: a tool for genome-scale analysis of protein functions and evolution journal January 2000
ProtTest: selection of best-fit models of protein evolution journal January 2005
Anaerobic respiration with elemental sulfur and with disulfides journal December 1998
A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea journal January 2017
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
KEGG as a reference resource for gene and protein annotation journal October 2015
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes journal May 2012
ARB: a software environment for sequence data journal February 2004
MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph preprint January 2014
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing journal May 2012
Extra virgin olive oil improved body weight and insulin sensitivity in high fat diet-induced obese LDLr−/−.Leiden mice without attenuation of steatohepatitis journal April 2021
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage journal July 2013
Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea journal March 2019
Accelerated Profile HMM Searches journal October 2011
Linking pangenomes and metagenomes: the Prochlorococcus metapangenome journal January 2018
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria journal April 2001
Metabolic, Phylogenetic, and Ecological Diversity of the Methanogenic Archaea journal March 2008
Diversity of Methane-Cycling Archaea in Hydrothermal Sediment Investigated by General and Group-Specific PCR Primers text January 2015
The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane journal June 2010
Thermophilic archaea activate butane via alkyl-coenzyme M formation journal October 2016
A marine microbial consortium apparently mediating anaerobic oxidation of methane journal October 2000
Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group journal February 2010
Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. journal August 1996
Basic local alignment search tool journal October 1990
Methanogenic archaea: ecologically relevant differences in energy conservation journal June 2008
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota journal October 2016
Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes journal June 2017
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space journal February 2012
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins journal March 2021
Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle journal February 2018
Zero-valent sulphur is a key intermediate in marine methane oxidation journal November 2012
Complex archaea that bridge the gap between prokaryotes and eukaryotes journal May 2015
Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria journal October 2015
Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction journal August 2017
Bacterial evolution. journal January 1987
Insights into the phylogeny and coding potential of microbial dark matter journal July 2013
Pfam: the protein families database journal November 2013
Metallosphaera sedula gen, and sp. nov. Represents a New Genus of Aerobic, Metal-Mobilizing, Thermoacidophilic Archaebacteria journal July 1989
Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments journal August 2017
Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases journal October 2014
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies text January 2014
Bacterial evolution journal June 1987

Cited By (3)

Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea journal October 2019
Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea journal March 2019
Metal-dependent anaerobic methane oxidation in marine sediment: Insights from marine settings and other systems journal June 2019

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