Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea

Abstract

Here, we report that sulfate is the predominant electron acceptor for anaerobic oxidation of methane (AOM) in marine sediments. This process is carried out by a syntrophic consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria (SRB) through an energy conservation mechanism that is still poorly understood. It was previously hypothesized that ANME alone could couple methane oxidation to dissimilatory sulfate reduction, but a genetic and biochemical basis for this proposal has not been identified. Using comparative genomic and phylogenetic analyses, we found the genetic capacity in ANME and related methanogenic archaea for sulfate reduction, including sulfate adenylyltransferase, APS kinase, APS/PAPS reductase and two different sulfite reductases. Additionally, based on characterized homologs and the lack of associated energy conserving complexes, the sulfate reduction pathways in ANME are likely used for assimilation but not dissimilation of sulfate. Environmental metaproteomic analysis confirmed the expression of 6 proteins in the sulfate assimilation pathway of ANME. The highest expressed proteins related to sulfate assimilation were two sulfite reductases, namely assimilatory-type low-molecular-weight sulfite reductase (alSir) and a divergent group of coenzyme F420-dependent sulfite reductase (Group II Fsr). In methane seep sediment microcosm experiments, however, sulfite and zero-valent sulfur amendments were inhibitory to ANME-2a/2c whilemore » growth in their syntrophic SRB partner was not observed. Combined with our genomic and metaproteomic results, the passage of sulfur species by ANME as metabolic intermediates for their SRB partners is unlikely. Instead, our findings point to a possible niche for ANME to assimilate inorganic sulfur compounds more oxidized than sulfide in anoxic marine environments.« less

Authors:
; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1484309
Alternate Identifier(s):
OSTI ID: 1528712
Grant/Contract Number:  
SC0016469; AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Yu, Hang, Susanti, Dwi, McGlynn, Shawn E., Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Scheller, Silvan, Tavormina, Patricia L., Hettich, Robert L., Mukhopadhyay, Biswarup, and Orphan, Victoria J. Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea. Switzerland: N. p., 2018. Web. doi:10.3389/fmicb.2018.02917.
Copy to clipboard
Yu, Hang, Susanti, Dwi, McGlynn, Shawn E., Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Scheller, Silvan, Tavormina, Patricia L., Hettich, Robert L., Mukhopadhyay, Biswarup, & Orphan, Victoria J. Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea. Switzerland. https://doi.org/10.3389/fmicb.2018.02917
Copy to clipboard
Yu, Hang, Susanti, Dwi, McGlynn, Shawn E., Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Scheller, Silvan, Tavormina, Patricia L., Hettich, Robert L., Mukhopadhyay, Biswarup, and Orphan, Victoria J. Mon . "Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea". Switzerland. https://doi.org/10.3389/fmicb.2018.02917.
Copy to clipboard
@article{osti_1484309,
title = {Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea},
author = {Yu, Hang and Susanti, Dwi and McGlynn, Shawn E. and Skennerton, Connor T. and Chourey, Karuna and Iyer, Ramsunder and Scheller, Silvan and Tavormina, Patricia L. and Hettich, Robert L. and Mukhopadhyay, Biswarup and Orphan, Victoria J.},
abstractNote = {Here, we report that sulfate is the predominant electron acceptor for anaerobic oxidation of methane (AOM) in marine sediments. This process is carried out by a syntrophic consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria (SRB) through an energy conservation mechanism that is still poorly understood. It was previously hypothesized that ANME alone could couple methane oxidation to dissimilatory sulfate reduction, but a genetic and biochemical basis for this proposal has not been identified. Using comparative genomic and phylogenetic analyses, we found the genetic capacity in ANME and related methanogenic archaea for sulfate reduction, including sulfate adenylyltransferase, APS kinase, APS/PAPS reductase and two different sulfite reductases. Additionally, based on characterized homologs and the lack of associated energy conserving complexes, the sulfate reduction pathways in ANME are likely used for assimilation but not dissimilation of sulfate. Environmental metaproteomic analysis confirmed the expression of 6 proteins in the sulfate assimilation pathway of ANME. The highest expressed proteins related to sulfate assimilation were two sulfite reductases, namely assimilatory-type low-molecular-weight sulfite reductase (alSir) and a divergent group of coenzyme F420-dependent sulfite reductase (Group II Fsr). In methane seep sediment microcosm experiments, however, sulfite and zero-valent sulfur amendments were inhibitory to ANME-2a/2c while growth in their syntrophic SRB partner was not observed. Combined with our genomic and metaproteomic results, the passage of sulfur species by ANME as metabolic intermediates for their SRB partners is unlikely. Instead, our findings point to a possible niche for ANME to assimilate inorganic sulfur compounds more oxidized than sulfide in anoxic marine environments.},
doi = {10.3389/fmicb.2018.02917},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {Switzerland},
year = {Mon Dec 03 00:00:00 EST 2018},
month = {Mon Dec 03 00:00:00 EST 2018}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.3389/fmicb.2018.02917
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 16 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Methanogens: a window into ancient sulfur metabolism
journal, May 2012

Structure of the Dissimilatory Sulfite Reductase from the Hyperthermophilic Archaeon Archaeoglobus fulgidus
journal, June 2008

  • Schiffer, Alexander; Parey, Kristian; Warkentin, Eberhard
  • Journal of Molecular Biology, Vol. 379, Issue 5
  • DOI: 10.1016/j.jmb.2008.04.027

Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters
journal, May 1969

Domain Evolution and Functional Diversification of Sulfite Reductases
journal, February 2005

  • Dhillon, Ashita; Goswami, Sulip; Riley, Monica
  • Astrobiology, Vol. 5, Issue 1
  • DOI: 10.1089/ast.2005.5.18

Structural basis for mRNA surveillance by archaeal Pelota and GTP-bound EF1α complex
journal, September 2010

  • Kobayashi, Kan; Kikuno, Izumi; Kuroha, Kazushige
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 41
  • DOI: 10.1073/pnas.1009598107

NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy
journal, November 2011

  • Pruitt, K. D.; Tatusova, T.; Brown, G. R.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1079

Adenosine 5'-Phosphosulfate Sulfotransferase and Adenosine 5'-Phosphosulfate Reductase Are Identical Enzymes
journal, January 2000

  • Suter, M.; von Ballmoos, P.; Kopriva, S.
  • Journal of Biological Chemistry, Vol. 275, Issue 2
  • DOI: 10.1074/jbc.275.2.930

Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction
journal, February 2016

Structural outline of the detailed mechanism for elongation factor Ts-mediated guanine nucleotide exchange on elongation factor Tu
journal, July 2015

  • Thirup, Søren S.; Van, Lan Bich; Nielsen, Tine K.
  • Journal of Structural Biology, Vol. 191, Issue 1
  • DOI: 10.1016/j.jsb.2015.06.011

I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010

  • Roy, Ambrish; Kucukural, Alper; Zhang, Yang
  • Nature Protocols, Vol. 5, Issue 4
  • DOI: 10.1038/nprot.2010.5

Methane-consuming archaebacteria in marine sediments
journal, April 1999

  • Hinrichs, Kai-Uwe; Hayes, John M.; Sylva, Sean P.
  • Nature, Vol. 398, Issue 6730
  • DOI: 10.1038/19751

Isolation of P590 from Methanosarcina barkeri: Evidence for the presence of sulfite reductase activity
journal, October 1982

  • Moura, JoséJ. G.; Moura, Isabel; Santos, Helena
  • Biochemical and Biophysical Research Communications, Vol. 108, Issue 3
  • DOI: 10.1016/0006-291X(82)92099-X

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014

The khmer software package: enabling efficient nucleotide sequence analysis
journal, January 2015

New perspectives on anaerobic methane oxidation
journal, October 2000

Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 1. Thermodynamic and physical constraints
journal, December 2009

  • Alperin, M. J.; Hoehler, T. M.
  • American Journal of Science, Vol. 309, Issue 10
  • DOI: 10.2475/10.2009.01

metaSPAdes: a new versatile metagenomic assembler
journal, March 2017

  • Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton
  • Genome Research, Vol. 27, Issue 5
  • DOI: 10.1101/gr.213959.116

IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015

Single cell activity reveals direct electron transfer in methanotrophic consortia
journal, September 2015

  • McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P.
  • Nature, Vol. 526, Issue 7574
  • DOI: 10.1038/nature15512

A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea
journal, December 2015

Cryptic CH4 cycling in the sulfate–methane transition of marine sediments apparently mediated by ANME-1 archaea
journal, September 2018

Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics
journal, September 2004

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Coupling a Detergent Lysis/Cleanup Methodology with Intact Protein Fractionation for Enhanced Proteome Characterization
journal, October 2012

  • Sharma, Ritin; Dill, Brian D.; Chourey, Karuna
  • Journal of Proteome Research, Vol. 11, Issue 12
  • DOI: 10.1021/pr300709k

Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics
journal, December 2010

  • Chourey, Karuna; Jansson, Janet; VerBerkmoes, Nathan
  • Journal of Proteome Research, Vol. 9, Issue 12
  • DOI: 10.1021/pr100787q

I-TASSER server for protein 3D structure prediction
journal, January 2008

Sulfite Reductase Structure at 1.6  : Evolution and Catalysis for Reduction of Inorganic Anions
journal, October 1995

Immunological detection of enzymes for sulfate reduction in anaerobic methane-oxidizing consortia: Localization of enzymes for sulfate reduction
journal, October 2012

  • Milucka, Jana; Widdel, Friedrich; Shima, Seigo
  • Environmental Microbiology, Vol. 15, Issue 5
  • DOI: 10.1111/1462-2920.12003

Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia
journal, June 2016

  • Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 28
  • DOI: 10.1073/pnas.1603757113

Proteomic Stable Isotope Probing Reveals Biosynthesis Dynamics of Slow Growing Methane Based Microbial Communities
journal, April 2016

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

A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea
journal, January 2011

  • Pereira, Inês A. Cardoso; Ramos, Ana Raquel; Grein, Fabian
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00069

Anaerobic Oxidation of Methane: Progress with an Unknown Process
journal, October 2009

Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors
journal, November 2006

  • Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 50
  • DOI: 10.1073/pnas.0606379103

InterPro in 2017—beyond protein family and domain annotations
journal, November 2016

  • Finn, Robert D.; Attwood, Teresa K.; Babbitt, Patricia C.
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1107

Properties of the Cysteine Residues and Iron−Sulfur Cluster of the Assimilatory 5‘-Adenylyl Sulfate Reductase from Pseudomonas aeruginosa †
journal, October 2004

  • Kim, Sung-Kun; Rahman, Afroza; Bick, Julie-Ann
  • Biochemistry, Vol. 43, Issue 42
  • DOI: 10.1021/bi048811t

Dosage-Dependent Proteome Response of Shewanella oneidensis MR-1 to Acute Chromate Challenge
journal, May 2007

  • Thompson, Melissa R.; VerBerkmoes, Nathan C.; Chourey, Karuna
  • Journal of Proteome Research, Vol. 6, Issue 5
  • DOI: 10.1021/pr060502x

Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Oceanic Methane Biogeochemistry
journal, February 2007

Rapid quantification and isotopic analysis of dissolved sulfur species: Quantification and isotopic analysis of dissolved sulfur species
journal, April 2017

  • Smith, Derek A.; Sessions, Alex L.; Dawson, Katherine S.
  • Rapid Communications in Mass Spectrometry, Vol. 31, Issue 9
  • DOI: 10.1002/rcm.7846

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

ARB: a software environment for sequence data
journal, February 2004

In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area
journal, May 2002

Methane Seep Carbonates Host Distinct, Diverse, and Dynamic Microbial Assemblages
journal, December 2015

  • Case, David H.; Pasulka, Alexis L.; Marlow, Jeffrey J.
  • mBio, Vol. 6, Issue 6
  • DOI: 10.1128/mBio.01348-15

SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock
journal, October 2016

  • Bagnoud, Alexandre; Chourey, Karuna; Hettich, Robert L.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12770

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
  • DOI: 10.1038/nature12375

Molecular Basis for G Protein Control of the Prokaryotic ATP Sulfurylase
journal, January 2006

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
  • DOI: 10.1111/1462-2920.14077

Sulfate Transporters in Dissimilatory Sulfate Reducing Microorganisms: A Comparative Genomics Analysis
journal, March 2018

Effect of Environmental Conditions on Sulfate Reduction with Methane as Electron Donor by an Eckernförde Bay Enrichment
journal, September 2009

  • Meulepas, Roel J. W.; Jagersma, Christian G.; Khadem, Ahmad F.
  • Environmental Science & Technology, Vol. 43, Issue 17
  • DOI: 10.1021/es900633c

A marine microbial consortium apparently mediating anaerobic oxidation of methane
journal, October 2000

  • Boetius, Antje; Ravenschlag, Katrin; Schubert, Carsten J.
  • Nature, Vol. 407, Issue 6804
  • DOI: 10.1038/35036572

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

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

An Intertwined Evolutionary History of Methanogenic Archaea and Sulfate Reduction
journal, September 2012

The Molecular Nature of the Hydrophilic Sulfur Prepared from Aqueous Sulfide and Sulfite (Selmi Sulfur Sol)
journal, May 1989

  • Steudel, Ralf; Göbel, Thomas; Holdt, Gabriele
  • Zeitschrift für Naturforschung B, Vol. 44, Issue 5
  • DOI: 10.1515/znb-1989-0504

MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012

  • Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
  • Systematic Biology, Vol. 61, Issue 3
  • DOI: 10.1093/sysbio/sys029

Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

Molecular Dynamics of the Shewanella oneidensis Response to Chromate Stress
journal, March 2006

  • Brown, Steven D.; Thompson, Melissa R.; VerBerkmoes, Nathan C.
  • Molecular & Cellular Proteomics, Vol. 5, Issue 6
  • DOI: 10.1074/mcp.M500394-MCP200

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

  • Milucka, Jana; Ferdelman, Timothy G.; Polerecky, Lubos
  • Nature, Vol. 491, Issue 7425
  • DOI: 10.1038/nature11656

GTPase Activation of ATP Sulfurylase: The Mechanism
journal, March 1994

  • Liu, Changxian; Martin, Eugene; Leyh, Thomas S.
  • Biochemistry, Vol. 33, Issue 8
  • DOI: 10.1021/bi00174a009

A Conserved Mechanism for Sulfonucleotide Reduction
journal, July 2005

Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria
journal, October 2015

  • Wegener, Gunter; Krukenberg, Viola; Riedel, Dietmar
  • Nature, Vol. 526, Issue 7574
  • DOI: 10.1038/nature15733

MyriMatch:  Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007

  • Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 6, Issue 2
  • DOI: 10.1021/pr0604054

Discovery of a novel adenosine 5′-phosphosulfate (APS) reductase from the methanarcheon Methanocaldococcus jannaschii
journal, January 2011

COFACTOR: an accurate comparative algorithm for structure-based protein function annotation
journal, May 2012

  • Roy, Ambrish; Yang, Jianyi; Zhang, Yang
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks372

The Crystal Structure of the Ribosome Bound to EF-Tu and Aminoacyl-tRNA
journal, October 2009

Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways
journal, December 2013

VizBin - an application for reference-independent visualization and human-augmented binning of metagenomic data
journal, January 2015

Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities
journal, January 2005

    Sort by:
    [ × clear filter / sort ]

    Similar Records in DOE PAGES and OSTI.GOV collections: