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Title: Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

Abstract

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota , none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

Authors:
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Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1863468
Alternate Identifier(s):
OSTI ID: 1838397; OSTI ID: 1865081
Grant/Contract Number:  
AC02-05CH11231; OCE-1563702/1536405
Resource Type:
Published Article
Journal Name:
PLoS Biology (Online)
Additional Journal Information:
Journal Name: PLoS Biology (Online) Journal Volume: 20 Journal Issue: 1; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Chadwick, Grayson L., Skennerton, Connor T., Laso-Pérez, Rafael, Leu, Andy O., Speth, Daan R., Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J., Woyke, Tanja, Hallam, Steven J., Tyson, Gene W., Wegener, Gunter, Boetius, Antje, Orphan, Victoria J., and Wang, ed., Fengping. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea. United States: N. p., 2022. Web. doi:10.1371/journal.pbio.3001508.
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Chadwick, Grayson L., Skennerton, Connor T., Laso-Pérez, Rafael, Leu, Andy O., Speth, Daan R., Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J., Woyke, Tanja, Hallam, Steven J., Tyson, Gene W., Wegener, Gunter, Boetius, Antje, Orphan, Victoria J., & Wang, ed., Fengping. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea. United States. https://doi.org/10.1371/journal.pbio.3001508
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Chadwick, Grayson L., Skennerton, Connor T., Laso-Pérez, Rafael, Leu, Andy O., Speth, Daan R., Yu, Hang, Morgan-Lang, Connor, Hatzenpichler, Roland, Goudeau, Danielle, Malmstrom, Rex, Brazelton, William J., Woyke, Tanja, Hallam, Steven J., Tyson, Gene W., Wegener, Gunter, Boetius, Antje, Orphan, Victoria J., and Wang, ed., Fengping. Wed . "Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea". United States. https://doi.org/10.1371/journal.pbio.3001508.
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@article{osti_1863468,
title = {Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea},
author = {Chadwick, Grayson L. and Skennerton, Connor T. and Laso-Pérez, Rafael and Leu, Andy O. and Speth, Daan R. and Yu, Hang and Morgan-Lang, Connor and Hatzenpichler, Roland and Goudeau, Danielle and Malmstrom, Rex and Brazelton, William J. and Woyke, Tanja and Hallam, Steven J. and Tyson, Gene W. and Wegener, Gunter and Boetius, Antje and Orphan, Victoria J. and Wang, ed., Fengping},
abstractNote = {The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota , none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.},
doi = {10.1371/journal.pbio.3001508},
journal = {PLoS Biology (Online)},
number = 1,
volume = 20,
place = {United States},
year = {Wed Jan 05 00:00:00 EST 2022},
month = {Wed Jan 05 00:00:00 EST 2022}
}
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Methanogenic capabilities of ANME-archaea deduced from 13 C-labelling approaches : Methanogenesis of ANME
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Trimmomatic: a flexible trimmer for Illumina sequence data
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The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
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MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph
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Methane- and Sulfur-Metabolizing Microbial Communities Dominate the Lost City Hydrothermal Field Ecosystem
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The prokaryotic Mo/W-bisPGD enzymes family: A catalytic workhorse in bioenergetic
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Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments
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metaSPAdes: a new versatile metagenomic assembler
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VhuD Facilitates Electron Flow from H2 or Formate to Heterodisulfide Reductase in Methanococcus maripaludis
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MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
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The structural basis for peptide selection by the transport receptor OppA
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A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
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Cryptic CH4 cycling in the sulfate–methane transition of marine sediments apparently mediated by ANME-1 archaea
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CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
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Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase
journal, June 2010

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The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems
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The Tetraheme Cytochrome CymA Is Required for Anaerobic Respiration with Dimethyl Sulfoxide and Nitrite in Shewanella oneidensis †
journal, August 2003

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The Expanding World of Methylotrophic Metabolism
journal, October 2009

Metabolic Capabilities of Microorganisms Involved in and Associated with the Anaerobic Oxidation of Methane
journal, February 2016

InterProScan 5: genome-scale protein function classification
journal, January 2014

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014

Characterization of two pterin derivatives isolated from Methanoculleus thermophilicum
journal, September 1991

Insights into Flavin-based Electron Bifurcation via the NADH-dependent Reduced Ferredoxin:NADP Oxidoreductase Structure
journal, July 2015

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  • Journal of Biological Chemistry, Vol. 290, Issue 36
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Contractile injection systems of bacteriophages and related systems: Conserved features of a contractile sheath-rigid tube mechanism
journal, February 2018

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  • Molecular Microbiology, Vol. 108, Issue 1
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GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database
journal, November 2019

A variant System I for cytochrome c biogenesis in archaea and some bacteria has a novel CcmE and no CcmH
journal, August 2006

Cohesin-dockerin microarray: Diverse specificities between two complementary families of interacting protein modules
journal, March 2008

Homocysteine Is Biosynthesized from Aspartate Semialdehyde and Hydrogen Sulfide in Methanogenic Archaea
journal, May 2015

Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella
journal, November 2011

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Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group
journal, February 2010

Partial Functional Replacement of CymA by SirCD in Shewanella oneidensis MR-1
journal, March 2011

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Investigation of serine hydroxymethyltransferase in methanogens
journal, July 1998

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Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life
journal, September 2017

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Structure of Coenzyme F420 Dependent Methylenetetrahydromethanopterin Reductase from Two Methanogenic Archaea
journal, July 2000

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Catalytic and Thermodynamic Properties of Tetrahydromethanopterin-dependent Serine Hydroxymethyltransferase from Methanococcus jannaschii
journal, October 2003

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Zero-valent sulphur is a key intermediate in marine methane oxidation
journal, November 2012

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Electron transport during aceticlastic methanogenesis by Methanosarcina acetivorans involves a sodium-translocating Rnf complex
journal, November 2012

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GroopM: an automated tool for the recovery of population genomes from related metagenomes
journal, January 2014

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MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

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Crystal structures and enzymatic properties of three formyltransferases from archaea: Environmental adaptation and evolutionary relationship
journal, September 2002

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Cellulosome-like sequences in Archaeoglobus fulgidus : an enigmatic vestige of cohesin and dockerin domains
journal, December 1999

Noncellulosomal cohesin- and dockerin-like modules in the three domains of life
journal, February 2009

De novo modeling of the F420-reducing [NiFe]-hydrogenase from a methanogenic archaeon by cryo-electron microscopy
journal, March 2013

Autotrophic Carbon Dioxide Fixation via the Calvin-Benson-Bassham Cycle by the Denitrifying Methanotroph “Candidatus Methylomirabilis oxyfera”
journal, February 2014

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  • Applied and Environmental Microbiology, Vol. 80, Issue 8
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Cytochrome c biogenesis: the Ccm system
journal, June 2010

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  • Trends in Microbiology, Vol. 18, Issue 6
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Flavin-Based Electron Bifurcation, A New Mechanism of Biological Energy Coupling
journal, February 2018

ggplot2
book, January 2009

Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium
journal, December 1994

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Structure of the F 420 H 2 :quinone oxidoreductase of Archaeoglobus fulgidus: Identification and overproduction of the F 420 H 2 -oxidizing subunit
journal, September 2000

Structure of the surface layer of the methanogenic archaean Methanosarcina acetivorans
journal, July 2012

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  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 29
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A Serpentinite-Hosted Ecosystem: The Lost City Hydrothermal Field
journal, March 2005

Function of coenzyme F 420 -dependent NADP reductase in methanogenic archaea containing an NADP-dependent alcohol dehydrogenase
journal, October 1997

Mechanisms Involved in Fe(III) Respiration by the Hyperthermophilic Archaeon Ferroglobus placidus
journal, February 2015

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Marine Tubeworm Metamorphosis Induced by Arrays of Bacterial Phage Tail–Like Structures
journal, January 2014

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One carbon metabolism in methanogenic bacteria: Cellular characterization and growth of Methanosarcina barkeri
journal, January 1978

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  • Archives of Microbiology, Vol. 119, Issue 1
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Archaea and bacteria with surprising microdiversity show shifts in dominance over 1,000-year time scales in hydrothermal chimneys
journal, January 2010

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  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 4
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Structure of a methyl-coenzyme M reductase from Black Sea mats that oxidize methane anaerobically
journal, November 2011

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  • Nature, Vol. 481, Issue 7379
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The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks
journal, November 2013

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Autotrophic carbon fixation in archaea
journal, May 2010

  • Berg, Ivan A.; Kockelkorn, Daniel; Ramos-Vera, W. Hugo
  • Nature Reviews Microbiology, Vol. 8, Issue 6, p. 447-460
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Electron transport in acetate-grown Methanosarcina acetivorans
journal, January 2011

An elusive electron shuttle from a facultative anaerobe
journal, June 2019

Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system
journal, March 2016

  • Speth, Daan R.; in ’t Zandt, Michiel H.; Guerrero-Cruz, Simon
  • Nature Communications, Vol. 7, Issue 1
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Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics
journal, September 2004

ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data
journal, February 2016

  • Huerta-Cepas, Jaime; Serra, François; Bork, Peer
  • Molecular Biology and Evolution, Vol. 33, Issue 6
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Genetic Basis for Metabolism of Methylated Sulfur Compounds in Methanosarcina Species
journal, February 2015

  • Fu, He; Metcalf, William W.
  • Journal of Bacteriology, Vol. 197, Issue 8
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Divergent Nrf Family Proteins and MtrCAB Homologs Facilitate Extracellular Electron Transfer in Aeromonas hydrophila
journal, September 2018

  • Conley, Bridget E.; Intile, Peter J.; Bond, Daniel R.
  • Applied and Environmental Microbiology, Vol. 84, Issue 23
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The archaeal cell envelope
journal, May 2011

  • Albers, Sonja-Verena; Meyer, Benjamin H.
  • Nature Reviews Microbiology, Vol. 9, Issue 6
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KBase: The United States Department of Energy Systems Biology Knowledgebase
journal, July 2018

  • Arkin, Adam P.; Cottingham, Robert W.; Henry, Christopher S.
  • Nature Biotechnology, Vol. 36, Issue 7
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Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments
journal, August 2017

A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction
journal, April 2018

Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage
journal, July 2013

  • Haroon, Mohamed F.; Hu, Shihu; Shi, Ying
  • Nature, Vol. 500, Issue 7464
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Evolutionary origins of members of a superfamily of integral membrane cytochrome c biogenesis proteins
journal, September 2007

  • Lee, Jong-Hoon; Harvat, Edgar M.; Stevens, Julie M.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 9
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Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia: Interspecies interaction within AOM consortia
journal, April 2018

  • Krukenberg, Viola; Riedel, Dietmar; Gruber-Vodicka, Harald R.
  • Environmental Microbiology, Vol. 20, Issue 5
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Consumption of Methane and CO2 by Methanotrophic Microbial Mats from Gas Seeps of the Anoxic Black Sea
journal, February 2007

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  • Applied and Environmental Microbiology, Vol. 73, Issue 7
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SMS: Smart Model Selection in PhyML
journal, May 2017

  • Lefort, Vincent; Longueville, Jean-Emmanuel; Gascuel, Olivier
  • Molecular Biology and Evolution, Vol. 34, Issue 9
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A marine microbial consortium apparently mediating anaerobic oxidation of methane
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  • Nature, Vol. 407, Issue 6804
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Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes
journal, January 2012

Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens
journal, July 2014

  • Welte, Cornelia; Deppenmeier, Uwe
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7
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Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis
journal, June 2018

The ‘porin-cytochrome’ model for microbe-to-mineral electron transfer: Microbe-to-mineral electron transfer
journal, May 2012

Divergent methyl-coenzyme M reductase genes in a deep-subseafloor Archaeoglobi
journal, January 2019

Extensive carbon isotopic heterogeneity among methane seep microbiota
journal, September 2009

Electron Transport in the Pathway of Acetate Conversion to Methane in the Marine Archaeon Methanosarcina acetivorans
journal, December 2005

An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
journal, November 2014

IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes
journal, October 2018

  • Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna
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Hydrogenases from Methanogenic Archaea, Nickel, a Novel Cofactor, and H 2 Storage
journal, June 2010

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