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Genomic composition and dynamics among Methanomicrobiales predict adaptation to contrasting environments

Journal Article · · The ISME Journal
 [1];  [2];  [3];  [3];  [4];  [5];  [6];  [7];  [8];  [7];  [9]
  1. Arizona State Univ., Tempe, AZ (United States); Aarhus Univ. (Denmark)
  2. National Inst. of Advanced Industrial Science and Technology (AIST), Ibaraki (Japan)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  5. Japan Agency for Marine-Earth Science and Technology, Kanagawa (Japan)
  6. Appalachian State Univ., Boone, NC (United States)
  7. Cornell Univ., Ithaca, NY (United States)
  8. Univ. of Illinois, Urbana-Champaign, IL (United States)
  9. Arizona State Univ., Tempe, AZ (United States)
+ Show Author Affiliations
Members of the order Methanomicrobiales are abundant, and sometimes dominant, hydrogenotrophic (H2-CO2 utilizing) methanoarchaea in a broad range of anoxic habitats. In spite of their key roles in greenhouse gas emissions and waste conversion to methane, little is known about the physiological and genomic bases for their widespread distribution and abundance. In this work, we compared the genomes of nine diverse Methanomicrobiales strains, examined their pangenomes, reconstructed gene flow and identified genes putatively mediating their success across different habitats. Most strains slowly increased gene content whereas one, Methanocorpusculum labreanum, evidenced genome downsizing. Peat-dwelling Methanomicrobiales showed adaptations centered on improved transport of scarce inorganic nutrients and likely use H+ rather than Na+ transmembrane chemiosmotic gradients during energy conservation. In contrast, other Methanomicrobiales show the potential to concurrently use Na+ and H+ chemiosmotic gradients. Analyses also revealed that the Methanomicrobiales lack a canonical electron bifurcation system (MvhABGD) known to produce low potential electrons in other orders of hydrogenotrophic methanogens. Additional putative differences in anabolic metabolism suggest that the dynamics of interspecies electron transfer from Methanomicrobiales syntrophic partners can also differ considerably. Altogether, our findings suggest profound differences in electron trafficking in the Methanomicrobiales compared with other hydrogenotrophs, and warrant further functional evaluations.
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:
1379646
Journal Information:
The ISME Journal, Journal Name: The ISME Journal Journal Issue: 1 Vol. 11; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (79)

Basic Local Alignment Search Tool journal October 1990
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton journal September 2000
Methanogenium, a new genus of marine methanogenic bacteria, and characterization ofMethanogenium cariaci sp. nov. andMethanogenium marisnigri sp. nov. journal May 1979
Methanoplanus limicola, a plate-shaped methanogen representing a novel family, the methanoplanaceae journal July 1982
Amelioration of Bacterial Genomes: Rates of Change and Exchange journal April 1997
The Kdp-ATPase system and its regulation journal April 2007
Kup is the major K + uptake system in Escherichia coli upon hyper-osmotic stress at a low pH journal March 1999
Basic local alignment search tool journal October 1990
An index of substitution saturation and its application journal January 2003
ATP synthases from archaea: The beauty of a molecular motor journal June 2014
Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass journal June 2011
A putative new order of methanogenic Archaea inhabiting the human gut, as revealed by molecular analyses of the mcrA gene journal September 2008
Lateral gene transfer and the nature of bacterial innovation journal May 2000
Global ecological patterns in uncultured Archaea journal October 2009
Functional responses of methanogenic archaea to syntrophic growth journal June 2012
Genomic and phenotypic differentiation among Methanosarcina mazei populations from Columbia River sediment journal March 2015
Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen journal March 2016
Isolation of a novel acidiphilic methanogen from an acidic peat bog journal May 2006
jModelTest 2: more models, new heuristics and parallel computing journal July 2012
Methanogenic archaea: ecologically relevant differences in energy conservation journal June 2008
Genomic islands in pathogenic and environmental microorganisms journal May 2004
Evolution of Na + and H + bioenergetics in methanogenic archaea journal February 2013
Functionally distinct genes regulated by hydrogen limitation and growth rate in methanogenic Archaea journal May 2007
Hydrogen is a preferred intermediate in the energy-conserving electron transport chain of Methanosarcina barkeri journal September 2009
Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase journal June 2010
Promiscuous archaeal ATP synthase concurrently coupled to Na+ and H+ translocation journal January 2012
Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis journal August 2012
Soil–Methanogen Interactions in Two Peatlands (Bog, Fen) in Central New York State journal July 2007
The impact of HGT on phylogenomic reconstruction methods journal August 2012
IslandPath: aiding detection of genomic islands in prokaryotes journal February 2003
Clustal W and Clustal X version 2.0 journal September 2007
Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood journal June 2010
ProtTest 3: fast selection of best-fit models of protein evolution journal February 2011
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods journal May 2011
DAMBE5: A Comprehensive Software Package for Data Analysis in Molecular Biology and Evolution journal April 2013
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 1999
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments journal July 2006
A novel host-specific restriction system associated with DNA backbone S-modification in Salmonella journal July 2010
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space journal February 2012
Transfer of Methanogenium bourgense, Methanogenium marisnigri, Methanogenium olentangyi, and Methanogenium thermophilicum to the Genus Methanoculleus gen. nov., Emendation of Methanoculleus marisnigri and Methanogenium, and Description of New Strains of Methanoculleus bourgense and Methanoculleus marisnigri journal April 1990
Methanosphaerula palustris gen. nov., sp. nov., a hydrogenotrophic methanogen isolated from a minerotrophic fen peatland journal April 2009
Methanoregula formicica sp. nov., a methane-producing archaeon isolated from methanogenic sludge journal August 2009
Methanoregula boonei gen. nov., sp. nov., an acidiphilic methanogen isolated from an acidic peat bog journal February 2010
Methanolinea tarda gen. nov., sp. nov., a methane-producing archaeon isolated from a methanogenic digester sludge journal January 2008
Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage 'Rice Cluster I', and proposal of the new archaeal order Methanocellales ord. nov. journal April 2008
Genome of Methanoregula boonei 6A8 reveals adaptations to oligotrophic peatland environments journal August 2015
Comparative genomics of three M ethanocellales strains reveal novel taxonomic and metabolic features : Comparative genomics of three journal April 2015
Evidence for the involvement of two heterodisulfide reductases in the energy-conserving system of Methanomassiliicoccus luminyensis journal December 2015
Methanogenesis by Methanosarcina acetivorans involves two structurally and functionally distinct classes of heterodisulfide reductase journal February 2010
Comparative transcriptome analysis of responses of Methanothermobacter thermautotrophicus to different environmental stimuli journal April 2008
Methanoplanus petrolearius sp. nov., a novel methanogenic bacterium from an oil-producing well journal February 1997
Genome Streamlining in a Cosmopolitan Oceanic Bacterium journal August 2005
Flagellum Mediates Symbiosis journal March 2009
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics journal October 2015
Energetics of syntrophic cooperation in methanogenic degradation. journal January 1997
Microbial Diversity in Natural Asphalts of the Rancho La Brea Tar Pits journal April 2007
Characterization of the Archaeal Community in a Minerotrophic Fen and Terminal Restriction Fragment Length Polymorphism-Directed Isolation of a Novel Hydrogenotrophic Methanogen journal February 2008
The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes journal September 2006
VhuD Facilitates Electron Flow from H2 or Formate to Heterodisulfide Reductase in Methanococcus maripaludis journal September 2013
The Genome Sequence of Methanosphaera stadtmanae Reveals Why This Human Intestinal Archaeon Is Restricted to Methanol and H2 for Methane Formation and ATP Synthesis journal December 2005
Complete Genome Sequence of Methanosphaerula palustris E1-9C T , a Hydrogenotrophic Methanogen Isolated from a Minerotrophic Fen Peatland journal November 2015
Evolution of Divergent Life History Strategies in Marine Alphaproteobacteria journal July 2013
K + , Na + , and Mg 2+ content and permeability of Methanospirillum hungatei and Methanobacterium thermoautotrophicum journal April 1981
Low-Temperature (10°C) Anaerobic Digestion of Dilute Dairy Wastewater in an EGSB Bioreactor: Microbial Community Structure, Population Dynamics, and Kinetics of Methanogenic Populations journal January 2013
Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models journal March 2006
Genome-wide evidence for positive selection and recombination in Actinobacillus pleuropneumoniae journal July 2011
Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine journal January 2014
Phylogenomic species tree estimation in the presence of incomplete lineage sorting and horizontal gene transfer journal January 2015
Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer journal January 2012
Methanogenesis in Marine Sediments journal March 2008
Resolving Difficult Phylogenetic Questions: Why More Sequences Are Not Enough journal March 2011
Repeated, Selection-Driven Genome Reduction of Accessory Genes in Experimental Populations journal May 2012
Genomic Characterization of Methanomicrobiales Reveals Three Classes of Methanogens journal June 2009
Comparative Proteomic Analysis of Methanothermobacter themautotrophicus ΔH in Pure Culture and in Co-Culture with a Butyrate-Oxidizing Bacterium journal August 2011
Halophilic microorganisms and adaptation to life at high salt concentrations – evolutionary aspects book December 2015
Genetic resources for methane production from biomass described with the Gene Ontology journal December 2014
Complete genome sequence of Methanocorpusculum labreanum type strain Z journal September 2009
Archaebiotics: Proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease journal October 2013

Cited By (3)

GC bias affects genomic and metagenomic reconstructions, underrepresenting GC-poor organisms journal February 2020
Robust Mercury Methylation across Diverse Methanogenic Archaea journal April 2018
Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis journal June 2018

Figures / Tables (7)

Table 1(p. 3)table Table 1
Figure1(p. 4)figure Figure1
Figure 2(p. 6)figure Figure 2
Figure 3(p. 6)figure Figure 3
Figure 4(p. 7)figure Figure 4
Figure 5(p. 7)figure Figure 5
Figure 6(p. 8)figure Figure 6

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Related Subjects

54 ENVIRONMENTAL SCIENCES
archaeal genomics
microbial ecology
molecular evolution