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Title: Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

Abstract

Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2 lineages. Metatranscriptome measurements in both communities indicated high levels of expression of genes for methane metabolism despite their distinct microbial communities and hydrocarbon composition. In contrast, the transcription level of sulfur cycle genes was quite different. In the thermogenic seep community, high levels of transcripts indicative of syntrophic anaerobic oxidation of methane (AOM) coupled to sulfate reduction were detected. This syntrophic partnership between the dominant ANME-2 and sulfate reducers potentially involves direct electron transfer through multiheme cytochromes. In the biogenic methane seep, genes from an ANME-1 lineage that are potentially involved in polysulfide reduction were highly expressed, suggesting a novelmore » bacterium-independent anaerobic methane oxidation pathway coupled to polysulfide reduction. The observed divergence in AOM activities provides a new model for bacterium-independent AOM and emphasizes the variation that exists in AOM pathways between different ANME lineages. IMPORTANCECold seep sediments are complex and widespread marine ecosystems emitting large amounts of methane, a potent greenhouse gas, and other hydrocarbons. Within these sediments, microbial communities play crucial roles in production and degradation of hydrocarbons, modulating oil and gas emissions to seawater. Despite this ecological importance, our understanding of microbial functions and methane oxidation pathways in cold seep ecosystems is poor. Based on gene expression profiling of environmental seep sediment samples, the present work showed that (i) the composition of the emitted fluids shapes the microbial community in general and the anaerobic methanotroph community specifically and (ii) AOM by ANME-2 in this seep may be coupled to sulfate reduction by Deltaproteobacteria by electron transfer through multiheme cytochromes, whereas AOM by ANME-1 lineages in this seep may involve a different, bacterium-independent pathway, coupling methane oxidation to elemental sulfur/polysulfide reduction.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [2];  [3];  [3];  [3];  [3];  [4];  [5];  [5];  [6];  [1];  [7]
  1. Newcastle Univ., Newcastle Upon Tyne (United Kingdom); Shell International Exploration and Production Inc., Houston, TX (United States)
  2. Laval Univ., Quebec City, QC (Canada)
  3. Shell International Exploration and Production Inc., Houston, TX (United States)
  4. Shell Global Solutions International B.V., Rijswijk (Netherlands)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Newcastle Univ., Newcastle Upon Tyne (United Kingdom)
  7. Univ. of British Columbia, Vancouver, BC (Canada)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1559175
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 4; Journal Issue: 1; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Vigneron, Adrien, Alsop, Eric B., Cruaud, Perrine, Philibert, Gwenaelle, King, Benjamin, Baksmaty, Leslie, Lavallee, David, Lomans, Bartholomeus P., Eloe-Fadrosh, Emiley, Kyrpides, Nikos C., Head, Ian M., Tsesmetzis, Nicolas, and Hallam, Steven J. Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments. United States: N. p., 2019. Web. doi:10.1128/mSystems.00091-18.
Vigneron, Adrien, Alsop, Eric B., Cruaud, Perrine, Philibert, Gwenaelle, King, Benjamin, Baksmaty, Leslie, Lavallee, David, Lomans, Bartholomeus P., Eloe-Fadrosh, Emiley, Kyrpides, Nikos C., Head, Ian M., Tsesmetzis, Nicolas, & Hallam, Steven J. Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments. United States. https://doi.org/10.1128/mSystems.00091-18
Vigneron, Adrien, Alsop, Eric B., Cruaud, Perrine, Philibert, Gwenaelle, King, Benjamin, Baksmaty, Leslie, Lavallee, David, Lomans, Bartholomeus P., Eloe-Fadrosh, Emiley, Kyrpides, Nikos C., Head, Ian M., Tsesmetzis, Nicolas, and Hallam, Steven J. Tue . "Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments". United States. https://doi.org/10.1128/mSystems.00091-18. https://www.osti.gov/servlets/purl/1559175.
@article{osti_1559175,
title = {Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments},
author = {Vigneron, Adrien and Alsop, Eric B. and Cruaud, Perrine and Philibert, Gwenaelle and King, Benjamin and Baksmaty, Leslie and Lavallee, David and Lomans, Bartholomeus P. and Eloe-Fadrosh, Emiley and Kyrpides, Nikos C. and Head, Ian M. and Tsesmetzis, Nicolas and Hallam, Steven J.},
abstractNote = {Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2 lineages. Metatranscriptome measurements in both communities indicated high levels of expression of genes for methane metabolism despite their distinct microbial communities and hydrocarbon composition. In contrast, the transcription level of sulfur cycle genes was quite different. In the thermogenic seep community, high levels of transcripts indicative of syntrophic anaerobic oxidation of methane (AOM) coupled to sulfate reduction were detected. This syntrophic partnership between the dominant ANME-2 and sulfate reducers potentially involves direct electron transfer through multiheme cytochromes. In the biogenic methane seep, genes from an ANME-1 lineage that are potentially involved in polysulfide reduction were highly expressed, suggesting a novel bacterium-independent anaerobic methane oxidation pathway coupled to polysulfide reduction. The observed divergence in AOM activities provides a new model for bacterium-independent AOM and emphasizes the variation that exists in AOM pathways between different ANME lineages. IMPORTANCECold seep sediments are complex and widespread marine ecosystems emitting large amounts of methane, a potent greenhouse gas, and other hydrocarbons. Within these sediments, microbial communities play crucial roles in production and degradation of hydrocarbons, modulating oil and gas emissions to seawater. Despite this ecological importance, our understanding of microbial functions and methane oxidation pathways in cold seep ecosystems is poor. Based on gene expression profiling of environmental seep sediment samples, the present work showed that (i) the composition of the emitted fluids shapes the microbial community in general and the anaerobic methanotroph community specifically and (ii) AOM by ANME-2 in this seep may be coupled to sulfate reduction by Deltaproteobacteria by electron transfer through multiheme cytochromes, whereas AOM by ANME-1 lineages in this seep may involve a different, bacterium-independent pathway, coupling methane oxidation to elemental sulfur/polysulfide reduction.},
doi = {10.1128/mSystems.00091-18},
journal = {mSystems},
number = 1,
volume = 4,
place = {United States},
year = {Tue Feb 26 00:00:00 EST 2019},
month = {Tue Feb 26 00:00:00 EST 2019}
}

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Works referenced in this record:

Feast and famine — microbial life in the deep-sea bed
journal, October 2007

  • Jørgensen, Bo Barker; Boetius, Antje
  • Nature Reviews Microbiology, Vol. 5, Issue 10
  • DOI: 10.1038/nrmicro1745

Structural and Molecular Genetic Insight into a Widespread Sulfur Oxidation Pathway
journal, December 2008

  • Dahl, Christiane; Schulte, Andrea; Stockdreher, Yvonne
  • Journal of Molecular Biology, Vol. 384, Issue 5
  • DOI: 10.1016/j.jmb.2008.10.016

Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink
journal, October 2006

  • Niemann, Helge; Lösekann, Tina; de Beer, Dirk
  • Nature, Vol. 443, Issue 7113
  • DOI: 10.1038/nature05227

Comparative metagenomics of hydrocarbon and methane seeps of the Gulf of Mexico
journal, November 2017


Microbial and Isotopic Evidence for Methane Cycling in Hydrocarbon-Containing Groundwater from the Pennsylvania Region
journal, April 2017


A microbial consortium couples anaerobic methane oxidation to denitrification
journal, April 2006

  • Raghoebarsing, Ashna A.; Pol, Arjan; van de Pas-Schoonen, Katinka T.
  • Nature, Vol. 440, Issue 7086
  • DOI: 10.1038/nature04617

Global dispersion and local diversification of the methane seep microbiome
journal, March 2015

  • Ruff, S. Emil; Biddle, Jennifer F.; Teske, Andreas P.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 13
  • DOI: 10.1073/pnas.1421865112

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


Manganese- and Iron-Dependent Marine Methane Oxidation
journal, July 2009


Reduction of molecular sulphur by methanogenic bacteria
journal, September 1983

  • Stetter, Karl O.; Gaag, Günther
  • Nature, Vol. 305, Issue 5932
  • DOI: 10.1038/305309a0

Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses
journal, July 2013

  • Blazewicz, Steven J.; Barnard, Romain L.; Daly, Rebecca A.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.102

MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
journal, April 2007

  • Tamura, K.; Dudley, J.; Nei, M.
  • Molecular Biology and Evolution, Vol. 24, Issue 8
  • DOI: 10.1093/molbev/msm092

Microbial impact on polysulfide dynamics in the environment
journal, April 2016


MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph
journal, January 2015


Archaea catalyze iron-dependent anaerobic oxidation of methane
journal, October 2016

  • Ettwig, Katharina F.; Zhu, Baoli; Speth, Daan
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 45
  • DOI: 10.1073/pnas.1609534113

Comparing and Evaluating Metagenome Assembly Tools from a Microbiologist’s Perspective - Not Only Size Matters!
journal, January 2017


Uncultured archaea in deep marine subsurface sediments: have we caught them all?
journal, November 2007


Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments
journal, May 2002

  • Orphan, V. J.; House, C. H.; Hinrichs, K.-U.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 11, p. 7663-7668
  • DOI: 10.1073/pnas.072210299

Microbial communities associated with benthic faunal assemblages at cold seep sediments of the Sonora Margin, Guaymas Basin
journal, August 2015


Reverse Methanogenesis and Respiration in Methanotrophic Archaea
journal, January 2017

  • Timmers, Peer H. A.; Welte, Cornelia U.; Koehorst, Jasper J.
  • Archaea, Vol. 2017
  • DOI: 10.1155/2017/1654237

Biogeochemical signatures and microbial activity of different cold-seep habitats along the Gulf of Mexico deep slope
journal, November 2010

  • Joye, Samantha B.; Bowles, Marshall W.; Samarkin, Vladimir A.
  • Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 57, Issue 21-23
  • DOI: 10.1016/j.dsr2.2010.06.001

Electron transfer in syntrophic communities of anaerobic bacteria and archaea
journal, August 2009

  • Stams, Alfons J. M.; Plugge, Caroline M.
  • Nature Reviews Microbiology, Vol. 7, Issue 8
  • DOI: 10.1038/nrmicro2166

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

Molecular biogeochemistry of sulfate reduction, methanogenesis and the anaerobic oxidation of methane at Gulf of Mexico cold seeps
journal, September 2005

  • Orcutt, Beth!; Boetius, Antje; Elvert, Marcus
  • Geochimica et Cosmochimica Acta, Vol. 69, Issue 17
  • DOI: 10.1016/j.gca.2005.04.012

Vulcanisaeta distributa gen. nov., sp. nov., and Vulcanisaeta souniana sp. nov., novel hyperthermophilic, rod-shaped crenarchaeotes isolated from hot springs in Japan.
journal, July 2002

  • Nakase, Takashi; Suzuki, Ken-ichiro; Itoh, Takashi
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 4
  • DOI: 10.1099/00207713-52-4-1097

Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011

  • Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
  • Nature Biotechnology, Vol. 29, Issue 7
  • DOI: 10.1038/nbt.1883

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


Energy Converting NADH: Quinone Oxidoreductase (Complex I)
journal, June 2006


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

Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments
journal, November 2010

  • Orcutt, Beth N.; Joye, Samantha B.; Kleindienst, Sara
  • Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 57, Issue 21-23
  • DOI: 10.1016/j.dsr2.2010.05.014

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

Genome-centric view of carbon processing in thawing permafrost
journal, July 2018


Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses
journal, September 2015

  • Dekas, Anne E.; Connon, Stephanie A.; Chadwick, Grayson L.
  • The ISME Journal, Vol. 10, Issue 3
  • DOI: 10.1038/ismej.2015.145

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


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


Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface
journal, November 2014

  • Probst, Alexander J.; Weinmaier, Thomas; Raymann, Kasie
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6497

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


Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments
journal, November 2011

  • Biddle, Jennifer F.; Cardman, Zena; Mendlovitz, Howard
  • The ISME Journal, Vol. 6, Issue 5
  • DOI: 10.1038/ismej.2011.164

IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies
journal, August 2012

  • Klindworth, Anna; Pruesse, Elmar; Schweer, Timmy
  • Nucleic Acids Research, Vol. 41, Issue 1
  • DOI: 10.1093/nar/gks808

MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002


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


SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB
journal, November 2007

  • Pruesse, E.; Quast, C.; Knittel, K.
  • Nucleic Acids Research, Vol. 35, Issue 21
  • DOI: 10.1093/nar/gkm864

Elemental sulfur reduction in the deep‐sea vent thermophile, Thermovibrio ammonificans
journal, June 2018

  • Jelen, Benjamin; Giovannelli, Donato; Falkowski, Paul G.
  • Environmental Microbiology, Vol. 20, Issue 6
  • DOI: 10.1111/1462-2920.14280

Application of metatranscriptomics to soil environments
journal, November 2012

  • Carvalhais, Lilia C.; Dennis, Paul G.; Tyson, Gene W.
  • Journal of Microbiological Methods, Vol. 91, Issue 2
  • DOI: 10.1016/j.mimet.2012.08.011

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

Xander: employing a novel method for efficient gene-targeted metagenomic assembly
journal, August 2015


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

Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics
journal, May 2008

  • Pernthaler, A.; Dekas, A. E.; Brown, C. T.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 19
  • DOI: 10.1073/pnas.0711303105

Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane
journal, September 1999


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


The effect of dissolved barium on biogeochemical processes at cold seeps
journal, April 2004

  • Aloisi, Giovanni; Wallmann, Klaus; Bollwerk, Sandra M.
  • Geochimica et Cosmochimica Acta, Vol. 68, Issue 8
  • DOI: 10.1016/j.gca.2003.10.010

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

Thermophilic anaerobic oxidation of methane by marine microbial consortia
journal, June 2011

  • Holler, Thomas; Widdel, Friedrich; Knittel, Katrin
  • The ISME Journal, Vol. 5, Issue 12
  • DOI: 10.1038/ismej.2011.77

Development of a new deep-sea hybrid Raman insertion probe and its application to the geochemistry of hydrothermal vent and cold seep fluids
journal, May 2017

  • Zhang, Xin; Du, Zengfeng; Zheng, Ronger
  • Deep Sea Research Part I: Oceanographic Research Papers, Vol. 123
  • DOI: 10.1016/j.dsr.2017.02.005

Archaeal and anaerobic methane oxidizer communities in the Sonora Margin cold seeps, Guaymas Basin (Gulf of California)
journal, February 2013

  • Vigneron, Adrien; Cruaud, Perrine; Pignet, Patricia
  • The ISME Journal, Vol. 7, Issue 8
  • DOI: 10.1038/ismej.2013.18

Diversity and Abundance of Aerobic and Anaerobic Methane Oxidizers at the Haakon Mosby Mud Volcano, Barents Sea
journal, March 2007

  • Losekann, T.; Knittel, K.; Nadalig, T.
  • Applied and Environmental Microbiology, Vol. 73, Issue 10
  • DOI: 10.1128/AEM.00016-07

Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia
journal, October 2009


In situ Identification of Ammonia-oxidizing Bacteria
journal, January 1995


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

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

Niche Separation of Methanotrophic Archaea (ANME-1 and -2) in Methane-Seep Sediments of the Eastern Japan Sea Offshore Joetsu
journal, February 2011

  • Yanagawa, Katsunori; Sunamura, Michinari; Lever, Mark Alexander
  • Geomicrobiology Journal, Vol. 28, Issue 2
  • DOI: 10.1080/01490451003709334

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

  • Imelfort, Michael; Parks, Donovan; Woodcroft, Ben J.
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.603

Novel insights into freshwater hydrocarbon-rich sediments using metatranscriptomics: Opening the black box
journal, June 2018


Spatial Structure and Activity of Sedimentary Microbial Communities Underlying a Beggiatoa spp. Mat in a Gulf of Mexico Hydrocarbon Seep
journal, January 2010


Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases
journal, October 2014

  • Müller, Albert Leopold; Kjeldsen, Kasper Urup; Rattei, Thomas
  • The ISME Journal, Vol. 9, Issue 5
  • DOI: 10.1038/ismej.2014.208

A new structure-based classification of sulfide:quinone oxidoreductases
journal, December 2009

  • Marcia, Marco; Ermler, Ulrich; Peng, Guohong
  • Proteins: Structure, Function, and Bioinformatics, Vol. 78, Issue 5, p. 1073-1083
  • DOI: 10.1002/prot.22665

IMG ER: a system for microbial genome annotation expert review and curation
journal, June 2009


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


DNA recovery from soils of diverse composition.
journal, January 1996


Potential application in amoxicillin removal of Alcaligenes sp. MMA and enzymatic studies through molecular docking
journal, March 2020

  • Sodhi, Kushneet Kaur; Kumar, Mohit; Singh, Dileep Kumar
  • Archives of Microbiology, Vol. 202, Issue 6
  • DOI: 10.1007/s00203-020-01868-1

Mimicking climate warming effects on Alaskan soil microbial communities via gradual temperature increase
journal, May 2020

  • Ballhausen, Max-Bernhard; Hewitt, Rebecca; Rillig, Matthias C.
  • Scientific Reports, Vol. 10, Issue 1
  • DOI: 10.1038/s41598-020-65329-x

Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments
text, January 2012

  • Zena, Cardman,; B., Albert, Daniel; Howard, Mendlovitz,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/6nv2-3796

Spatial Structure and Activity of Sedimentary Microbial Communities Underlying a Beggiatoa spp. Mat in a Gulf of Mexico Hydrocarbon Seep
text, January 2010

  • G., Lloyd, Karen; F., Biddle, Jennifer; B., Albert, Daniel
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/9tra-t647

Thermophilic anaerobic oxidation of methane by marine microbial consortia
text, January 2011

  • Andreas, Teske,; Y., Kellermann, Matthias; Gunter, Wegener,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/ttyb-qm72

Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink
text, January 2006


Global dispersion and local diversification of the methane seep microbiome
text, January 2015

  • Teske, Andreas P.; Ramette, Alban Nicolas; Boetius, Antje
  • National Academy of Sciences NAS
  • DOI: 10.7892/boris.91364

Diversity and Abundance of Aerobic and Anaerobic Methane Oxidizers at the Haakon Mosby Mud Volcano, Barents Sea
text, January 2007


Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments
text, January 2010

  • Ramette, Alban Nicolas; Boetius, Antje; Samarkin, Vladimir
  • Elsevier Science
  • DOI: 10.7892/boris.91399