Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep

Yu, Hang; Speth, Daan R.; Connon, Stephanie A.; Goudeau, Danielle; Malmstrom, Rex R.; Woyke, Tanja; Orphan, Victoria J.

doi:10.1128/aem.02109-21

Title: Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep

Journal Article · Mon May 23 00:00:00 EDT 2022 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/aem.02109-21· OSTI ID:1960231

^[1];

^[1]; Connon, Stephanie A. ^[1]; Goudeau, Danielle ^[2]; Malmstrom, Rex R. ^[2];

^[2]; Orphan, Victoria J. ^[1]

California Institute of Technology (CalTech), Pasadena, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States).Joint Genome Institute

We report Syntrophic consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) consume large amounts of methane and serve as the foundational microorganisms in marine methane seeps. Despite their importance in the carbon cycle, research on the physiology of ANME-SRB consortia has been hampered by the slow growth and complex physicochemical environment the consortia inhabit. Here, we report successful sediment-free enrichment of ANME-SRB consortia from deep-sea methane seep sediments in the Santa Monica Basin, California. Anoxic Percoll density gradients and size-selective filtration were used to separate ANME-SRB consortia from sediment particles and single cells to accelerate the cultivation process. Over a 3-year period, a subset of the sediment-associated ANME and SRB lineages, predominantly comprised of ANME-2a/2b (“Candidatus Methanocomedenaceae”) and their syntrophic bacterial partners, SEEP-SRB1/2, adapted and grew under defined laboratory conditions. Metagenome-assembled genomes from several enrichments revealed that ANME-2a, SEEP-SRB1, and Methanococcoides in different enrichments from the same inoculum represented distinct species, whereas other coenriched microorganisms were closely related at the species level. This suggests that ANME, SRB, and Methanococcoides are more genetically diverse than other members in methane seeps. Flow cytometry sorting and sequencing of cell aggregates revealed that Methanococcoides, Anaerolineales, and SEEP-SRB1 were overrepresented in multiple ANME-2a cell aggregates relative to the bulk metagenomes, suggesting they were physically associated and possibly interacting. Overall, this study represents a successful case of selective cultivation of anaerobic slow-growing microorganisms from sediments based on their physical characteristics, introducing new opportunities for detailed genomic, physiological, biochemical, and ecological analyses. Biological anaerobic oxidation of methane (AOM) coupled with sulfate reduction represents a large methane sink in global ocean sediments. Methane consumption is carried out by syntrophic archaeal-bacterial consortia and fuels a unique ecosystem, yet the interactions in these slow-growing syntrophic consortia and with other associated community members remain poorly understood. The significance of this study is the establishment of sediment-free enrichment cultures of anaerobic methanotrophic archaea and sulfate-reducing bacteria performing AOM with sulfate using selective cultivation approaches based on size, density, and metabolism. By reconstructing microbial genomes and analyzing community composition of the enrichment cultures and cell aggregates, we shed light on the diversity of microorganisms physically associated with AOM consortia beyond the core syntrophic partners. These enrichment cultures offer simplified model systems to extend our understanding of the diversity of microbial interactions within marine methane seeps.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Netherlands Organisation for Scientific Research

Grant/Contract Number:: AC02-05CH11231; SC0016469; 019.153LW.039

OSTI ID:: 1960231

Journal Information:: Applied and Environmental Microbiology, Vol. 88, Issue 11; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (88)

Microbial interactions: from networks to models Faust, Karoline; Raes, Jeroen Nature Reviews Microbiology, Vol. 10, Issue 8 https://doi.org/10.1038/nrmicro2832	journal	July 2012
Bacterial chemolithoautotrophy via manganese oxidation Yu, Hang; Leadbetter, Jared R. Nature, Vol. 583, Issue 7816 https://doi.org/10.1038/s41586-020-2468-5	journal	July 2020
Characterization of microbial associations with methanotrophic archaea and sulfate-reducing bacteria through statistical comparison of nested Magneto-FISH enrichments Trembath-Reichert, Elizabeth; Case, David H.; Orphan, Victoria J. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.1913	journal	January 2016
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters Cline, Joel D. Limnology and Oceanography, Vol. 14, Issue 3, p. 454-458 https://doi.org/10.4319/lo.1969.14.3.0454	journal	May 1969
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
"Candidatus Cloacamonas Acidaminovorans": Genome Sequence Reconstruction Provides a First Glimpse of a New Bacterial Division Pelletier, E.; Kreimeyer, A.; Bocs, S. Journal of Bacteriology, Vol. 190, Issue 7 https://doi.org/10.1128/JB.01248-07	journal	February 2008
In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate Nauhaus, Katja; Albrecht, Melanie; Elvert, Marcus Environmental Microbiology, Vol. 9, Issue 1 https://doi.org/10.1111/j.1462-2920.2006.01127.x	journal	January 2007
Stimulation of in vitro anaerobic oxidation of methane rate in a continuous high-pressure bioreactor Zhang, Yu; Henriet, Jean-Pierre; Bursens, Jeroen Bioresource Technology, Vol. 101, Issue 9 https://doi.org/10.1016/j.biortech.2009.11.103	journal	May 2010
Genomic and enzymatic evidence of acetogenesis by anaerobic methanotrophic archaea Yang, Shanshan; Lv, Yongxin; Liu, Xipeng Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17860-8	journal	August 2020
Variations in Archaeal and Bacterial Diversity Associated with the Sulfate-Methane Transition Zone in Continental Margin Sediments (Santa Barbara Basin, California) Harrison, B. K.; Zhang, H.; Berelson, W. Applied and Environmental Microbiology, Vol. 75, Issue 6 https://doi.org/10.1128/AEM.01812-08	journal	January 2009
Global dispersion and local diversification of the methane seep microbiome Ruff, S. Emil; Biddle, Jennifer F.; Teske, Andreas P. Proceedings of the National Academy of Sciences, Vol. 112, Issue 13 https://doi.org/10.1073/pnas.1421865112	journal	March 2015
The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation Allen, Michelle A.; Lauro, Federico M.; Williams, Timothy J. The ISME Journal, Vol. 3, Issue 9 https://doi.org/10.1038/ismej.2009.45	journal	April 2009
Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction Scheller, S.; Yu, H.; Chadwick, G. L. Science, Vol. 351, Issue 6274 https://doi.org/10.1126/science.aad7154	journal	February 2016
Candidatus Desulfofervidus auxilii, a hydrogenotrophic sulfate-reducing bacterium involved in the thermophilic anaerobic oxidation of methane : The partner bacterium in thermophilic methanotrophy Krukenberg, Viola; Harding, Katie; Richter, Michael Environmental Microbiology, Vol. 18, Issue 9 https://doi.org/10.1111/1462-2920.13283	journal	April 2016
A Methanogenic Archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Franzmann, P. D.; Springer, N.; Ludwig, W. Systematic and Applied Microbiology, Vol. 15, Issue 4 https://doi.org/10.1016/S0723-2020(11)80117-7	journal	December 1992
Enrichment of anaerobic methanotrophs in sulfate-reducing membrane bioreactors Meulepas, Roel J. W.; Jagersma, Christian G.; Gieteling, Jarno Biotechnology and Bioengineering, Vol. 104, Issue 3 https://doi.org/10.1002/bit.22412	journal	October 2009
New cell extraction procedure applied to deep subsurface sediments: Cell extraction of deep subsurface sediments Kallmeyer, Jens; Smith, David C.; Spivack, Arthur J. Limnology and Oceanography: Methods, Vol. 6, Issue 6 https://doi.org/10.4319/lom.2008.6.236	journal	June 2008
Enrichment of sulfate reducing anaerobic methane oxidizing community dominated by ANME-1 from Ginsburg Mud Volcano (Gulf of Cadiz) sediment in a biotrickling filter Bhattarai, Susma; Cassarini, Chiara; Rene, Eldon R. Bioresource Technology, Vol. 259 https://doi.org/10.1016/j.biortech.2018.03.018	journal	July 2018
Critical Assessment of Metagenome Interpretation—a benchmark of metagenomics software Sczyrba, Alexander; Hofmann, Peter; Belmann, Peter Nature Methods, Vol. 14, Issue 11 https://doi.org/10.1038/nmeth.4458	journal	October 2017
Patterns of ¹⁵ N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS Orphan, Victoria J.; Turk, Kendra A.; Green, Abigail M. Environmental Microbiology, Vol. 11, Issue 7 https://doi.org/10.1111/j.1462-2920.2009.01903.x	journal	July 2009
Methane Seep in Shallow-Water Permeable Sediment Harbors High Diversity of Anaerobic Methanotrophic Communities, Elba, Italy Ruff, S. Emil; Kuhfuss, Hanna; Wegener, Gunter Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00374	journal	March 2016
Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi Yamada, T. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 6 https://doi.org/10.1099/ijs.0.64169-0	journal	June 2006
Double Labeling of Oligonucleotide Probes for Fluorescence In Situ Hybridization (DOPE-FISH) Improves Signal Intensity and Increases rRNA Accessibility Stoecker, K.; Dorninger, C.; Daims, H. Applied and Environmental Microbiology, Vol. 76, Issue 3 https://doi.org/10.1128/AEM.02456-09	journal	December 2009
Anaerobic methane oxidation in metalliferous hydrothermal sediments: influence on carbon flux and decoupling from sulfate reduction: Anaerobic methane oxidation in hydrothermal vents Wankel, Scott D.; Adams, Melissa M.; Johnston, David T. Environmental Microbiology, Vol. 14, Issue 10 https://doi.org/10.1111/j.1462-2920.2012.02825.x	journal	July 2012
Microbes trading electricity in consortia of environmental and biotechnological significance Rotaru, Amelia-Elena; Yee, Mon Oo; Musat, Florin Current Opinion in Biotechnology, Vol. 67 https://doi.org/10.1016/j.copbio.2021.01.014	journal	February 2021
Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments Orphan, V. J.; House, C. H.; Hinrichs, K.-U. Proceedings of the National Academy of Sciences, Vol. 99, Issue 11, p. 7663-7668 https://doi.org/10.1073/pnas.072210299	journal	May 2002
Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides Manz, Werner; Eisenbrecher, Michael; Neu, Thomas R. FEMS Microbiology Ecology, Vol. 25, Issue 1 https://doi.org/10.1111/j.1574-6941.1998.tb00459.x	journal	January 1998
Enrichment and cultivation of prokaryotes associated with the sulphate-methane transition zone of diffusion-controlled sediments of Aarhus Bay, Denmark, under heterotrophic conditions: Enrichment of prokaryotes associated with the SMTZ Webster, Gordon; Sass, Henrik; Cragg, Barry A. FEMS Microbiology Ecology, Vol. 77, Issue 2 https://doi.org/10.1111/j.1574-6941.2011.01109.x	journal	May 2011
A sediment flow-through system to study the impact of shifting fluid and methane flow regimes on the efficiency of the benthic methane filter Steeb, Philip; Linke, Peter; Treude, Tina Limnology and Oceanography: Methods, Vol. 12, Issue 1 https://doi.org/10.4319/lom.2014.12.25	journal	January 2014
An experimental study on short-term changes in the anaerobic oxidation of methane in response to varying methane and sulfate fluxes Wegener, G.; Boetius, A. Biogeosciences, Vol. 6, Issue 5 https://doi.org/10.5194/bg-6-867-2009	journal	January 2009
Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system Speth, Daan R.; in ’t Zandt, Michiel H.; Guerrero-Cruz, Simon Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11172	journal	March 2016
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life Parks, Donovan H.; Chuvochina, Maria; Waite, David W. Nature Biotechnology, Vol. 36, Issue 10 https://doi.org/10.1038/nbt.4229	journal	August 2018
Missing lithotroph identified as new planctomycete Strous, Marc; Fuerst, John A.; Kramer, Evelien H. M. Nature, Vol. 400, Issue 6743 https://doi.org/10.1038/22749	journal	July 1999
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik Nature Reviews Microbiology, Vol. 16, Issue 10 https://doi.org/10.1038/s41579-018-0076-2	journal	September 2018
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont Huber, Harald; Hohn, Michael J.; Rachel, Reinhard Nature, Vol. 417, Issue 6884 https://doi.org/10.1038/417063a	journal	May 2002
Biogenic formation of amorphous carbon by anaerobic methanotrophs and select methanogens Allen, Kylie D.; Wegener, Gunter; Matthew Sublett, D. Science Advances, Vol. 7, Issue 44 https://doi.org/10.1126/sciadv.abg9739	journal	October 2021
Comparative Genomics and Proteomic Analysis of Assimilatory Sulfate Reduction Pathways in Anaerobic Methanotrophic Archaea Yu, Hang; Susanti, Dwi; McGlynn, Shawn E. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02917	journal	December 2018
Bellilinea caldifistulae gen. nov., sp. nov. and Longilinea arvoryzae gen. nov., sp. nov., strictly anaerobic, filamentous bacteria of the phylum Chloroflexi isolated from methanogenic propionate-degrading consortia Yamada, Takeshi; Imachi, Hiroyuki; Ohashi, Akiyoshi International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 10 https://doi.org/10.1099/ijs.0.65098-0	journal	October 2007
Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle Proceedings of the National Academy of Sciences, Vol. 113, Issue 28 https://doi.org/10.1073/pnas.1603757113	journal	June 2016
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea Chadwick, Grayson L.; Skennerton, Connor T.; Laso-Pérez, Rafael PLOS Biology, Vol. 20, Issue 1 https://doi.org/10.1371/journal.pbio.3001508	journal	January 2022
Metabolic Capabilities of Microorganisms Involved in and Associated with the Anaerobic Oxidation of Methane Wegener, Gunter; Krukenberg, Viola; Ruff, S. Emil Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00046	journal	February 2016
Anaerobic Oxidation of Methane: Progress with an Unknown Process Knittel, Katrin; Boetius, Antje Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093130	journal	October 2009
Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C. Current Biology, Vol. 25, Issue 6 https://doi.org/10.1016/j.cub.2015.01.014	journal	March 2015
Identification of a Redox Active Thioquinoxalinol Sulfate Compound Produced by an Anaerobic Methane-Oxidizing Microbial Consortium White, Robert H.; Allen, Kylie D.; Wegener, Gunter ACS Omega, Vol. 4, Issue 27 https://doi.org/10.1021/acsomega.9b03450	journal	December 2019
Sulfate differentially stimulates but is not respired by diverse anaerobic methanotrophic archaea Yu, Hang; Skennerton, Connor T.; Chadwick, Grayson L. The ISME Journal, Vol. 16, Issue 1 https://doi.org/10.1038/s41396-021-01047-0	journal	July 2021
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Microbial diversity and community structure of a highly active anaerobic methane-oxidizing sulfate-reducing enrichment Jagersma, G. Christian; Meulepas, Roel J. W.; Heikamp-de Jong, Ineke Environmental Microbiology, Vol. 11, Issue 12 https://doi.org/10.1111/j.1462-2920.2009.02036.x	journal	December 2009
Enrichment of ANME-2 dominated anaerobic methanotrophy from cold seep sediment in an external ultrafiltration membrane bioreactor Bhattarai, Susma; Cassarini, Chiara; Rene, Eldon R. Engineering in Life Sciences, Vol. 18, Issue 6 https://doi.org/10.1002/elsc.201700148	journal	March 2018
Diversity and Distribution of Methanotrophic Archaea at Cold Seeps Knittel, K.; Losekann, T.; Boetius, A. Applied and Environmental Microbiology, Vol. 71, Issue 1 https://doi.org/10.1128/AEM.71.1.467-479.2005	journal	January 2005
Isolation and characterization of methylotrophic methanogens from anoxic marine sediments in Skan Bay, Alaska: description of Methanococcoides alaskense sp. nov., and emended description of Methanosarcina baltica Singh, N. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 6 https://doi.org/10.1099/ijs.0.63886-0	journal	November 2005
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Growth and Population Dynamics of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a Continuous-Flow Bioreactor Girguis, P. R.; Cozen, A. E.; DeLong, E. F. Applied and Environmental Microbiology, Vol. 71, Issue 7 https://doi.org/10.1128/AEM.71.7.3725-3733.2005	journal	July 2005
Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle He, Xuesong; McLean, Jeffrey S.; Edlund, Anna Proceedings of the National Academy of Sciences, Vol. 112, Issue 1 https://doi.org/10.1073/pnas.1419038112	journal	December 2014
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Growth of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a High-Pressure Membrane Capsule Bioreactor Timmers, Peer H. A.; Gieteling, Jarno; Widjaja-Greefkes, H. C. Aura Applied and Environmental Microbiology, Vol. 81, Issue 4 https://doi.org/10.1128/AEM.03255-14	journal	December 2014
Genomic insights into members of the candidate phylum Hyd24-12 common in mesophilic anaerobic digesters Kirkegaard, Rasmus Hansen; Dueholm, Morten Simonsen; McIlroy, Simon Jon The ISME Journal, Vol. 10, Issue 10 https://doi.org/10.1038/ismej.2016.43	journal	April 2016
Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics Pernthaler, A.; Dekas, A. E.; Brown, C. T. Proceedings of the National Academy of Sciences, Vol. 105, Issue 19 https://doi.org/10.1073/pnas.0711303105	journal	May 2008
The globally widespread genus Sulfurimonas: versatile energy metabolisms and adaptations to redox clines Han, Yuchen; Perner, Mirjam Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00989	journal	September 2015
Thermophilic archaea activate butane via alkyl-coenzyme M formation Laso-Pérez, Rafael; Wegener, Gunter; Knittel, Katrin Nature, Vol. 539, Issue 7629 https://doi.org/10.1038/nature20152	journal	October 2016
High-pressure systems for gas-phase free continuous incubation of enriched marine microbial communities performing anaerobic oxidation of methane Deusner, Christian; Meyer, Volker; Ferdelman, Timothy G. Biotechnology and Bioengineering, Vol. 105, Issue 3 https://doi.org/10.1002/bit.22553	journal	February 2010
A marine microbial consortium apparently mediating anaerobic oxidation of methane Boetius, Antje; Ravenschlag, Katrin; Schubert, Carsten J. Nature, Vol. 407, Issue 6804 https://doi.org/10.1038/35036572	journal	October 2000
Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor Girguis, P. R.; Orphan, V. J.; Hallam, S. J. Applied and Environmental Microbiology, Vol. 69, Issue 9 https://doi.org/10.1128/AEM.69.9.5472-5482.2003	journal	September 2003
The Impact of Methane on Microbial Communities at Marine Arctic Gas Hydrate Bearing Sediment Carrier, Vincent; Svenning, Mette M.; Gründger, Friederike Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01932	journal	September 2020
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.126	journal	July 2017
Thermophilic anaerobic oxidation of methane by marine microbial consortia Holler, Thomas; Widdel, Friedrich; Knittel, Katrin The ISME Journal, Vol. 5, Issue 12 https://doi.org/10.1038/ismej.2011.77	journal	June 2011
Candidatus Syntrophosphaera thermopropionivorans: a novel player in syntrophic propionate oxidation during anaerobic digestion Dyksma, Stefan; Gallert, Claudia Environmental Microbiology Reports, Vol. 11, Issue 4 https://doi.org/10.1111/1758-2229.12759	journal	April 2019
Erratum for Skennerton et al., “Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea” Skennerton, Connor T.; Chourey, Karuna; Iyer, Ramsunder mBio, Vol. 8, Issue 5 https://doi.org/10.1128/mBio.01561-17	journal	November 2017
Culture-Independent Analyses Reveal Novel Anaerolineaceae as Abundant Primary Fermenters in Anaerobic Digesters Treating Waste Activated Sludge McIlroy, Simon J.; Kirkegaard, Rasmus H.; Dueholm, Morten S. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01134	journal	June 2017
Comparison of Archaeal and Bacterial Diversity in Methane Seep Carbonate Nodules and Host Sediments, Eel River Basin and Hydrate Ridge, USA Mason, Olivia U.; Case, David H.; Naehr, Thomas H. Microbial Ecology, Vol. 70, Issue 3 https://doi.org/10.1007/s00248-015-0615-6	journal	May 2015
Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade: SEEP-SRB1 associated with ANME-2 Schreiber, Lars; Holler, Thomas; Knittel, Katrin Environmental Microbiology https://doi.org/10.1111/j.1462-2920.2010.02275.x	journal	July 2010
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky901	journal	October 2018
Growth and mechanism of filamentous-sulfur formation by Candidatus Arcobacter sulfidicus in opposing oxygen-sulfide gradients Sievert, Stefan M.; Wieringa, Elze B. A.; Wirsen, Carl O. Environmental Microbiology, Vol. 9, Issue 1 https://doi.org/10.1111/j.1462-2920.2006.01156.x	journal	January 2007
Enrichment of a microbial community performing anaerobic oxidation of methane in a continuous high-pressure bioreactor Zhang, Yu; Maignien, Loïs; Zhao, Xianxian BMC Microbiology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2180-11-137	journal	June 2011
Methanococcoides vulcani sp. nov., a marine methylotrophic methanogen that uses betaine, choline and N,N-dimethylethanolamine for methanogenesis, isolated from a mud volcano, and emended description of the genus Methanococcoides L'Haridon, S.; Chalopin, M.; Colombo, D. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 6 https://doi.org/10.1099/ijs.0.058289-0	journal	March 2014
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep Chen, Song-Can; Musat, Niculina; Lechtenfeld, Oliver J. Nature, Vol. 568, Issue 7750 https://doi.org/10.1038/s41586-019-1063-0	journal	March 2019
A Long-Term Cultivation of an Anaerobic Methane-Oxidizing Microbial Community from Deep-Sea Methane-Seep Sediment Using a Continuous-Flow Bioreactor Aoki, Masataka; Ehara, Masayuki; Saito, Yumi PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0105356	journal	August 2014
Crystal structure of a key enzyme for anaerobic ethane activation Hahn, Cedric J.; Lemaire, Olivier N.; Kahnt, Jörg Science, Vol. 373, Issue 6550 https://doi.org/10.1126/science.abg1765	journal	July 2021
Methane-Consuming Archaea Revealed by Directly Coupled Isotopic and Phylogenetic Analysis Orphan, V. J. Science, Vol. 293, Issue 5529 https://doi.org/10.1126/science.1061338	journal	July 2001
Insights into the ecology, evolution, and metabolism of the widespread Woesearchaeotal lineages Liu, Xiaobo; Li, Meng; Castelle, Cindy J. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0488-2	journal	June 2018
High Frequency of Thermodesulfovibrio spp. and Anaerolineaceae in Association with Methanoculleus spp. in a Long-Term Incubation of n-Alkanes-Degrading Methanogenic Enrichment Culture Liang, Bo; Wang, Li-Ying; Zhou, Zhichao Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01431	journal	September 2016
Putative Extracellular Electron Transfer in Methanogenic Archaea Gao, Kailin; Lu, Yahai Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.611739	journal	March 2021
Isolation and characterization of Flexilinea flocculi gen. nov., sp. nov., a filamentous, anaerobic bacterium belonging to the class Anaerolineae in the phylum Chloroflexi Sun, Liwei; Toyonaga, Mayu; Ohashi, Akiko International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 2 https://doi.org/10.1099/ijsem.0.000822	journal	February 2016

Similar Records

DOE new players Carbon cycle (2016-2021)

Technical Report · Sun Jun 12 00:00:00 EDT 2022 · OSTI ID:1960231

Orphan, Victoria Jeanne; Tyson, Gene; Meile, Christof; +3 more

Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea

Journal Article · Mon Sep 25 00:00:00 EDT 2023 · PLoS Biology (Online) · OSTI ID:1960231

Murali, Ranjani; Yu, Hang; Speth, Daan R.; +12 more

Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea

Journal Article · Tue Aug 01 00:00:00 EDT 2017 · mBio (Online) · OSTI ID:1960231

Skennerton, Connor T.; Chourey, Karuna; Iyer, Ramsunder; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
anaerobic oxidation of methane
anaerobic methanotrophic archaea
ANME
cultivation
flow cytometry
genomics
interspecies interaction

Title: Community Structure and Microbial Associations in Sediment-Free Methanotrophic Enrichment Cultures from a Marine Methane Seep

Citation Formats

References (88)

Similar Records

Related Subjects