Experimentally-validated correlation analysis reveals new anaerobic methane oxidation partnerships with consortium-level heterogeneity in diazotrophy

Metcalfe, Kyle S.; Murali, Ranjani; Mullin, Sean W.; Connon, Stephanie A.; Orphan, Victoria J.

doi:10.1038/s41396-020-00757-1

Title: Experimentally-validated correlation analysis reveals new anaerobic methane oxidation partnerships with consortium-level heterogeneity in diazotrophy

Journal Article · 15 October 2020 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-020-00757-1 · OSTI ID:1675016

^[1]; Murali, Ranjani ^[1];

^[1]; Connon, Stephanie A. ^[1];

^[1]

California Institute of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences

Archaeal anaerobic methanotrophs (“ANME”) and sulfate-reducing Deltaproteobacteria (“SRB”) form symbiotic multicellular consortia capable of anaerobic methane oxidation (AOM), and in so doing modulate methane flux from marine sediments. The specificity with which ANME associate with particular SRB partners in situ, however, is poorly understood. To characterize partnership specificity in ANME-SRB consortia, we applied the correlation inference technique SparCC to 310 16S rRNA amplicon libraries prepared from Costa Rica seep sediment samples, uncovering a strong positive correlation between ANME-2b and members of a clade of Deltaproteobacteria we termed SEEP-SRB1g. We confirmed this association by examining 16S rRNA diversity in individual ANME-SRB consortia sorted using flow cytometry and by imaging ANME-SRB consortia with fluorescence in situ hybridization (FISH) microscopy using newly-designed probes targeting the SEEP-SRB1g clade. Analysis of genome bins belonging to SEEP-SRB1g revealed the presence of a completenifHDKoperon required for diazotrophy, unusual in published genomes of ANME-associated SRB. Active expression ofnifHin SEEP-SRB1g within ANME-2b—SEEP-SRB1g consortia was then demonstrated by microscopy using hybridization chain reaction (HCR-) FISH targetingnifHtranscripts and diazotrophic activity was documented by FISH-nanoSIMS experiments. NanoSIMS analysis of ANME-2b—SEEP-SRB1g consortia incubated with a headspace containing CH₄and¹⁵N₂revealed differences in cellular¹⁵N-enrichment between the two partners that varied between individual consortia, with SEEP-SRB1g cells enriched in¹⁵N relative to ANME-2b in one consortium and the opposite pattern observed in others, indicating both ANME-2b and SEEP-SRB1g are capable of nitrogen fixation, but with consortium-specific variation in whether the archaea or bacterial partner is the dominant diazotroph.

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Research Organization:: California Institute of Technology (CalTech), Pasadena, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; USDOE

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0020373

OSTI ID:: 1675016

Alternate ID(s):: OSTI ID: 1816486

Journal Information:: The ISME Journal, Vol. 15, Issue 2; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (103)

Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink Niemann, Helge; Lösekann, Tina; de Beer, Dirk Nature, Vol. 443, Issue 7113 https://doi.org/10.1038/nature05227	journal	October 2006
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
Evidence for phylogenetically and catabolically diverse active diazotrophs in deep-sea sediment Kapili, Bennett J.; Barnett, Samuel E.; Buckley, Daniel H. The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0584-8	journal	January 2020
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
Nitrogen fixation in sediments along a depth transect through the Peruvian oxygen minimum zone Gier, Jessica; Sommer, Stefan; Löscher, Carolin R. Biogeosciences, Vol. 13, Issue 14 https://doi.org/10.5194/bg-13-4065-2016	journal	January 2016
A microbial consortium couples anaerobic methane oxidation to denitrification Raghoebarsing, Ashna A.; Pol, Arjan; van de Pas-Schoonen, Katinka T. Nature, Vol. 440, Issue 7086 https://doi.org/10.1038/nature04617	journal	April 2006
Microbial Reefs in the Black Sea Fueled by Anaerobic Oxidation of Methane Michaelis, W. Science, Vol. 297, Issue 5583 https://doi.org/10.1126/science.1072502	journal	August 2002
Exposing the Three-Dimensional Biogeography and Metabolic States of Pathogens in Cystic Fibrosis Sputum via Hydrogel Embedding, Clearing, and rRNA Labeling DePas, William H.; Starwalt-Lee, Ruth; Van Sambeek, Lindsey mBio, Vol. 7, Issue 5 https://doi.org/10.1128/mBio.00796-16	journal	September 2016
Methane-consuming archaebacteria in marine sediments Hinrichs, Kai-Uwe; Hayes, John M.; Sylva, Sean P. Nature, Vol. 398, Issue 6730 https://doi.org/10.1038/19751	journal	April 1999
Bacterioplankton Compositions of Lakes and Oceans: a First Comparison Based on Fluorescence In Situ Hybridization Glöckner, Frank Oliver; Fuchs, Bernhard M.; Amann, Rudolf Applied and Environmental Microbiology, Vol. 65, Issue 8 https://doi.org/10.1128/AEM.65.8.3721-3726.1999	journal	August 1999
Environmental control on anaerobic oxidation of methane in the gassy sediments of Eckernförde Bay (German Baltic) Treude, Tina; Krüger, Martin; Boetius, Antje Limnology and Oceanography, Vol. 50, Issue 6 https://doi.org/10.4319/lo.2005.50.6.1771	journal	November 2005
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
The Natural History of Nitrogen Fixation Raymond, Jason; Siefert, Janet L.; Staples, Christopher R. Molecular Biology and Evolution, Vol. 21, Issue 3 https://doi.org/10.1093/molbev/msh047	journal	March 2004
Inferring Correlation Networks from Genomic Survey Data Friedman, Jonathan; Alm, Eric J. PLoS Computational Biology, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pcbi.1002687	journal	September 2012
Sparse and Compositionally Robust Inference of Microbial Ecological Networks Kurtz, Zachary D.; Müller, Christian L.; Miraldi, Emily R. PLOS Computational Biology, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pcbi.1004226	journal	May 2015
Single cell activity reveals direct electron transfer in methanotrophic consortia McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P. Nature, Vol. 526, Issue 7574 https://doi.org/10.1038/nature15512	journal	September 2015
A functional perspective on phenotypic heterogeneity in microorganisms Ackermann, Martin Nature Reviews Microbiology, Vol. 13, Issue 8 https://doi.org/10.1038/nrmicro3491	journal	July 2015
Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy McGlynn, Shawn E.; Chadwick, Grayson L.; O'Neill, Ariel Applied and Environmental Microbiology, Vol. 84, Issue 11 https://doi.org/10.1128/AEM.00399-18	journal	April 2018
From The Cover: Triggered amplification by hybridization chain reaction Dirks, R. M.; Pierce, N. A. Proceedings of the National Academy of Sciences, Vol. 101, Issue 43 https://doi.org/10.1073/pnas.0407024101	journal	October 2004
Lineage-Specific Transcriptional Profiles of Symbiodinium spp. Unaltered by Heat Stress in a Coral Host Barshis, Daniel J.; Ladner, Jason T.; Oliver, Thomas A. Molecular Biology and Evolution, Vol. 31, Issue 6 https://doi.org/10.1093/molbev/msu107	journal	March 2014
Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments : Sulfate-reducing bacteria at marine hydrocarbon seeps Kleindienst, Sara; Ramette, Alban; Amann, Rudolf Environmental Microbiology, Vol. 14, Issue 10 https://doi.org/10.1111/j.1462-2920.2012.02832.x	journal	August 2012
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
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
Spatial distribution of nitrogen fixation in methane seep sediment and the role of the ANME archaea: Nitrogen fixation in methane seep sediment Dekas, Anne E.; Chadwick, Grayson L.; Bowles, Marshall W. Environmental Microbiology, Vol. 16, Issue 10 https://doi.org/10.1111/1462-2920.12247	journal	September 2013
circlize implements and enhances circular visualization in R Gu, Zuguang; Gu, Lei; Eils, Roland Bioinformatics, Vol. 30, Issue 19 https://doi.org/10.1093/bioinformatics/btu393	journal	June 2014
Oceanic Methane Biogeochemistry Reeburgh, William S. Chemical Reviews, Vol. 107, Issue 2 https://doi.org/10.1021/cr050362v	journal	February 2007
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Next-Generation in Situ Hybridization Chain Reaction: Higher Gain, Lower Cost, Greater Durability Choi, Harry M. T.; Beck, Victor A.; Pierce, Niles A. ACS Nano, Vol. 8, Issue 5 https://doi.org/10.1021/nn405717p	journal	April 2014
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
The Contamination of Commercial 15N2 Gas Stocks with 15N–Labeled Nitrate and Ammonium and Consequences for Nitrogen Fixation Measurements Dabundo, Richard; Lehmann, Moritz F.; Treibergs, Lija PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0110335	journal	October 2014
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
Graph drawing by force-directed placement Fruchterman, Thomas M. J.; Reingold, Edward M. Software: Practice and Experience, Vol. 21, Issue 11 https://doi.org/10.1002/spe.4380211102	journal	November 1991
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
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
Illumina-based analysis of microbial community diversity Degnan, Patrick H.; Ochman, Howard The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.74	journal	June 2011
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
Activity of abundant and rare bacteria in a coastal ocean Campbell, B. J.; Yu, L.; Heidelberg, J. F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 31 https://doi.org/10.1073/pnas.1101405108	journal	July 2011
Microbiome Datasets Are Compositional: And This Is Not Optional Gloor, Gregory B.; Macklaim, Jean M.; Pawlowsky-Glahn, Vera Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02224	journal	November 2017
Archaeal and anaerobic methane oxidizer communities in the Sonora Margin cold seeps, Guaymas Basin (Gulf of California) Vigneron, Adrien; Cruaud, Perrine; Pignet, Patricia The ISME Journal, Vol. 7, Issue 8 https://doi.org/10.1038/ismej.2013.18	journal	February 2013
Widespread fluid expulsion along the seafloor of the Costa Rica convergent margin: Fluid expulsion along the Costa Rican convergent margin Bohrmann, Gerhard; Heeschen, Katja; Jung, Carmen Terra Nova, Vol. 14, Issue 2 https://doi.org/10.1046/j.1365-3121.2002.00400.x	journal	April 2002
Occurrence of benthic microbial nitrogen fixation coupled to sulfate reduction in the seasonally hypoxic Eckernförde Bay, Baltic Sea Bertics, V. J.; Löscher, C. R.; Salonen, I. Biogeosciences, Vol. 10, Issue 3 https://doi.org/10.5194/bg-10-1243-2013	journal	January 2013
Isolation of an archaeon at the prokaryote–eukaryote interface Imachi, Hiroyuki; Nobu, Masaru K.; Nakahara, Nozomi Nature, Vol. 577, Issue 7791 https://doi.org/10.1038/s41586-019-1916-6	journal	January 2020
Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria Wegener, Gunter; Krukenberg, Viola; Riedel, Dietmar Nature, Vol. 526, Issue 7574 https://doi.org/10.1038/nature15733	journal	October 2015
Environmental control on anaerobic oxidation of methane in the gassy sediments of Eckernförde Bay (German Baltic) Treude, Tina; Krüger, Martin; Boetius, Antje Limnology and Oceanography, Vol. 50, Issue 6 https://doi.org/10.4319/lo.2005.50.6.1771	journal	November 2005
Interactive Tree Of Life (iTOL) v4: recent updates and new developments Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz239	journal	April 2019
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
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
Concepts for biocontrol in marine environments: is there a way forward? Atalah, Javier; Hopkins, Grant; Fletcher, Lauren Management of Biological Invasions, Vol. 6, Issue 1 https://doi.org/10.3391/mbi.2015.6.1.01	journal	March 2015
Reaction–diffusion model of nutrient uptake in a biofilm: Theory and experiment Petroff, Alexander P.; Wu, Ting-Di; Liang, Biqing Journal of Theoretical Biology, Vol. 289 https://doi.org/10.1016/j.jtbi.2011.08.004	journal	November 2011
Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink Niemann, Helge; Lösekann, Tina; de Beer, Dirk Nature, Vol. 443, Issue 7113 https://doi.org/10.1038/nature05227	journal	October 2006
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
Look@NanoSIMS - a tool for the analysis of nanoSIMS data in environmental microbiology: Look@NanoSIMS Polerecky, Lubos; Adam, Birgit; Milucka, Jana Environmental Microbiology, Vol. 14, Issue 4 https://doi.org/10.1111/j.1462-2920.2011.02681.x	journal	January 2012
Determinants of community structure in the global plankton interactome Lima-Mendez, G.; Faust, K.; Henry, N. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1262073	journal	May 2015
A microbial consortium couples anaerobic methane oxidation to denitrification Raghoebarsing, Ashna A.; Pol, Arjan; van de Pas-Schoonen, Katinka T. Nature, Vol. 440, Issue 7086 https://doi.org/10.1038/nature04617	journal	April 2006
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
Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type Sampayo, E. M.; Ridgway, T.; Bongaerts, P. Proceedings of the National Academy of Sciences, Vol. 105, Issue 30 https://doi.org/10.1073/pnas.0708049105	journal	July 2008
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
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
An evolving view of methane metabolism in the Archaea Evans, Paul N.; Boyd, Joel A.; Leu, Andy O. Nature Reviews Microbiology, Vol. 17, Issue 4 https://doi.org/10.1038/s41579-018-0136-7	journal	January 2019
Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies Klawonn, Isabell; Eichner, Meri J.; Wilson, Samuel T. The ISME Journal, Vol. 14, Issue 2 https://doi.org/10.1038/s41396-019-0514-9	journal	October 2019
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
Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane Green-Saxena, A.; Dekas, A. E.; Dalleska, N. F. The ISME Journal, Vol. 8, Issue 1 https://doi.org/10.1038/ismej.2013.147	journal	September 2013
Geochemical, metagenomic and metaproteomic insights into trace metal utilization by methane-oxidizing microbial consortia in sulphidic marine sediments: Metal micronutrients for anaerobic oxidation of methane Glass, Jennifer B.; Yu, Hang; Steele, Joshua A. Environmental Microbiology, Vol. 16, Issue 6 https://doi.org/10.1111/1462-2920.12314	journal	November 2013
Nitrogen fixation in sediments along a depth transect through the Peruvian oxygen minimum zone Gier, Jessica; Sommer, Stefan; Löscher, Carolin R. Biogeosciences, Vol. 13, Issue 14 https://doi.org/10.5194/bg-13-4065-2016	journal	January 2016
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
XSEDE: Accelerating Scientific Discovery Towns, John; Cockerill, Timothy; Dahan, Maytal Computing in Science & Engineering, Vol. 16, Issue 5 https://doi.org/10.1109/MCSE.2014.80	journal	September 2014
Gene Expression Variation Resolves Species and Individual Strains among Coral-Associated Dinoflagellates within the Genus Symbiodinium Parkinson, John E.; Baumgarten, Sebastian; Michell, Craig T. Genome Biology and Evolution, Vol. 8, Issue 3 https://doi.org/10.1093/gbe/evw019	journal	February 2016
Widespread nitrogen fixation in sediments from diverse deep‐sea sites of elevated carbon loading Dekas, Anne E.; Fike, David A.; Chadwick, Grayson L. Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14342	journal	July 2018
Phenotypic heterogeneity driven by nutrient limitation promotes growth in fluctuating environments Schreiber, Frank; Littmann, Sten; Lavik, Gaute Nature Microbiology, Vol. 1, Issue 6 https://doi.org/10.1038/nmicrobiol.2016.55	journal	May 2016
Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses Dekas, Anne E.; Connon, Stephanie A.; Chadwick, Grayson L. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.145	journal	September 2015
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
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
Occurrence of benthic microbial nitrogen fixation coupled to sulfate reduction in the seasonally hypoxic Eckernförde Bay, Baltic Sea Bertics, V. J.; Löscher, C. R.; Salonen, I. Biogeosciences, Vol. 10, Issue 3 https://doi.org/10.5194/bg-10-1243-2013	journal	January 2013
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
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
Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea Hallam, S. J.; Girguis, P. R.; Preston, C. M. Applied and Environmental Microbiology, Vol. 69, Issue 9 https://doi.org/10.1128/AEM.69.9.5483-5491.2003	journal	September 2003
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage Haroon, Mohamed F.; Hu, Shihu; Shi, Ying Nature, Vol. 500, Issue 7464 https://doi.org/10.1038/nature12375	journal	July 2013
Comparative Analysis of Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in Anoxic Marine Sediments Orphan, V. J.; Hinrichs, K. -U.; Ussler, W. Applied and Environmental Microbiology, Vol. 67, Issue 4 https://doi.org/10.1128/AEM.67.4.1922-1934.2001	journal	April 2001
Heterogeneous nitrogen fixation rates confer energetic advantage and expanded ecological niche of unicellular diazotroph populations Masuda, Takako; Inomura, Keisuke; Takahata, Naoto Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-0894-4	journal	April 2020
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
Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia: Interspecies interaction within AOM consortia Krukenberg, Viola; Riedel, Dietmar; Gruber-Vodicka, Harald R. Environmental Microbiology, Vol. 20, Issue 5 https://doi.org/10.1111/1462-2920.14077	journal	April 2018
Oligonucleotide Microarray for 16S rRNA Gene-Based Detection of All Recognized Lineages of Sulfate-Reducing Prokaryotes in the Environment Loy, A.; Lehner, A.; Lee, N. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/AEM.68.10.5064-5081.2002	journal	October 2002
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
Deciphering microbial interactions and detecting keystone species with co-occurrence networks Berry, David; Widder, Stefanie Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00219	journal	May 2014
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
A Bayesian method for detecting pairwise associations in compositional data Schwager, Emma; Mallick, Himel; Ventz, Steffen PLOS Computational Biology, Vol. 13, Issue 11 https://doi.org/10.1371/journal.pcbi.1005852	journal	November 2017
Effects of Diurnal Variation of Gut Microbes and High-Fat Feeding on Host Circadian Clock Function and Metabolism Leone, Vanessa; Gibbons, Sean M.; Martinez, Kristina Cell Host & Microbe, Vol. 17, Issue 5 https://doi.org/10.1016/j.chom.2015.03.006	journal	May 2015
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
Diversity and Abundance of Aerobic and Anaerobic Methane Oxidizers at the Haakon Mosby Mud Volcano, Barents Sea Losekann, T.; Knittel, K.; Nadalig, T. Applied and Environmental Microbiology, Vol. 73, Issue 10 https://doi.org/10.1128/AEM.00016-07	journal	March 2007
Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia Dekas, A. E.; Poretsky, R. S.; Orphan, V. J. Science, Vol. 326, Issue 5951 https://doi.org/10.1126/science.1178223	journal	October 2009
Fluid seepage at the continental margin offshore Costa Rica and southern Nicaragua: CONTINENTAL MARGIN FLUID SEEPAGE Sahling, Heiko; Masson, Douglas G.; Ranero, César R. Geochemistry, Geophysics, Geosystems, Vol. 9, Issue 5 https://doi.org/10.1029/2008GC001978	journal	May 2008
Diet rapidly and reproducibly alters the human gut microbiome David, Lawrence A.; Maurice, Corinne F.; Carmody, Rachel N. Nature, Vol. 505, Issue 7484 https://doi.org/10.1038/nature12820	journal	December 2013
Archaeal and anaerobic methane oxidizer communities in the Sonora Margin cold seeps, Guaymas Basin (Gulf of California) Vigneron, Adrien; Cruaud, Perrine; Pignet, Patricia The ISME Journal, Vol. 7, Issue 8 https://doi.org/10.1038/ismej.2013.18	journal	February 2013
A guided tour into subcellular colocalization analysis in light microscopy Bolte, S.; CordeliÈRes, F. P. Journal of Microscopy, Vol. 224, Issue 3 https://doi.org/10.1111/j.1365-2818.2006.01706.x	journal	December 2006
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
Estimates of methane output from mud extrusions at the erosive convergent margin off Costa Rica Mau, S.; Sahling, H.; Rehder, G. Marine Geology, Vol. 225, Issue 1-4 https://doi.org/10.1016/j.margeo.2005.09.007	journal	January 2006
In situ DNA-hybridization chain reaction (HCR): a facilitated in situ HCR system for the detection of environmental microorganisms: In situ DNA-HCR for environmental microorganisms Yamaguchi, Tsuyoshi; Kawakami, Shuji; Hatamoto, Masashi Environmental Microbiology, Vol. 17, Issue 7 https://doi.org/10.1111/1462-2920.12745	journal	February 2015
Structural Cohesion and Embeddedness: A Hierarchical Concept of Social Groups Moody, James; White, Douglas R. American Sociological Review, Vol. 68, Issue 1 https://doi.org/10.2307/3088904	journal	February 2003
Use of Hybridization Chain Reaction-Fluorescent In Situ Hybridization To Track Gene Expression by Both Partners during Initiation of Symbiosis Nikolakakis, K.; Lehnert, E.; McFall-Ngai, M. J. Applied and Environmental Microbiology, Vol. 81, Issue 14 https://doi.org/10.1128/AEM.00890-15	journal	May 2015
Whole Cell Immunomagnetic Enrichment of Environmental Microbial Consortia Using rRNA-Targeted Magneto-FISH Trembath-Reichert, Elizabeth; Green-Saxena, Abigail; Orphan, Victoria J. Methods in Enzymology https://doi.org/10.1016/B978-0-12-407863-5.00002-2	book	September 2013
Methane Seep Carbonates Host Distinct, Diverse, and Dynamic Microbial Assemblages Case, David H.; Pasulka, Alexis L.; Marlow, Jeffrey J. mBio, Vol. 6, Issue 6 https://doi.org/10.1128/mBio.01348-15	journal	December 2015
Creating the CIPRES Science Gateway for inference of large phylogenetic trees Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri 2010 Gateway Computing Environments Workshop (GCE) https://doi.org/10.1109/GCE.2010.5676129	conference	November 2010
Third-generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust Choi, Harry M. T.; Schwarzkopf, Maayan; Fornace, Mark E. Development, Vol. 145, Issue 12 https://doi.org/10.1242/dev.165753	journal	June 2018

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