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

Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle; Malmstrom, Rex R.; Woyke, Tanja; Orphan, Victoria J.

doi:10.1073/pnas.1603757113

Title: Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

Journal Article · Tue Jun 28 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1603757113· OSTI ID:1259913

Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle; Malmstrom, Rex R.; Woyke, Tanja; Orphan, Victoria J.

To understand the biogeochemical roles of microorganisms in the environment, it is important to determine when and under which conditions they are metabolically active. Bioorthogonal noncanonical amino acid tagging (BONCAT) can reveal active cells by tracking the incorporation of synthetic amino acids into newly synthesized proteins. The phylogenetic identity of translationally active cells can be determined by combining BONCAT with rRNA-targeted fluorescence in situ hybridization (BONCAT-FISH). In theory, BONCAT-labeled cells could be isolated with fluorescence-activated cell sorting (BONCAT-FACS) for subsequent genetic analyses. Here, in the first application, to our knowledge, of BONCAT-FISH and BONCAT-FACS within an environmental context, we probe the translational activity of microbial consortia catalyzing the anaerobic oxidation of methane (AOM), a dominant sink of methane in the ocean. These consortia, which typically are composed of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria, have been difficult to study due to their slow in situ growth rates, and fundamental questions remain about their ecology and diversity of interactions occurring between ANME and associated partners. Our activity-correlated analyses of > 16,400 microbial aggregates provide the first evidence, to our knowledge, that AOM consortia affiliated with all five major ANME clades are concurrently active under controlled conditions. Surprisingly, sorting of individual BONCAT-labeled consortia followed by whole-genome amplification and 16S rRNA gene sequencing revealed previously unrecognized interactions of ANME with members of the poorly understood phylum Verrucomicrobia. This finding, together with our observation that ANME-associated Verrucomicrobia are found in a variety of geographically distinct methane seep environments, suggests a broader range of symbiotic relationships within AOM consortia than previously thought.

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Austrian Science Fund (FWF); Gordon and Betty Moore Foundation

Grant/Contract Number:: AC02-05CH11231; OCE-0825791; GBMF3780

OSTI ID:: 1259913

Alternate ID(s):: OSTI ID: 1379511

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 113 Journal Issue: 28; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 113 works

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References (91)

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
Detection of Protein-Synthesizing Microorganisms in the Environment via Bioorthogonal Noncanonical Amino Acid Tagging (BONCAT) Hatzenpichler, Roland; Orphan, Victoria J. Springer Protocols Handbooks https://doi.org/10.1007/8623_2015_61	book	January 2015
A thermodynamic analysis of the anaerobic oxidation of methane in marine sediments Larowe, D. E.; Dale, A. W.; Regnier, P. Geobiology, Vol. 6, Issue 5 https://doi.org/10.1111/j.1472-4669.2008.00170.x	journal	December 2008
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
In Situ Accessibility of Small-Subunit rRNA of Members of the Domains Bacteria, Archaea, and Eucarya to Cy3-Labeled Oligonucleotide Probes Behrens, S.; Ruhland, C.; Inacio, J. Applied and Environmental Microbiology, Vol. 69, Issue 3 https://doi.org/10.1128/AEM.69.3.1748-1758.2003	journal	March 2003
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
Combination of Fluorescent In Situ Hybridization and Microautoradiography—a New Tool for Structure-Function Analyses in Microbial Ecology Lee, Natuscka; Nielsen, Per Halkjær; Andreasen, Kjær Holm Applied and Environmental Microbiology, Vol. 65, Issue 3 https://doi.org/10.1128/AEM.65.3.1289-1297.1999	journal	March 1999
Real-time detection of actively metabolizing microbes by redox sensing as applied to methylotroph populations in Lake Washington Kalyuzhnaya, Marina G.; Lidstrom, Mary E.; Chistoserdova, Ludmila The ISME Journal, Vol. 2, Issue 7 https://doi.org/10.1038/ismej.2008.32	journal	March 2008
Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function Huang, Wei E.; Stoecker, Kilian; Griffiths, Robert Environmental Microbiology, Vol. 9, Issue 8 https://doi.org/10.1111/j.1462-2920.2007.01352.x	journal	August 2007
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
Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation Kiick, K. L.; Saxon, E.; Tirrell, D. A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 1, p. 19-24 https://doi.org/10.1073/pnas.012583299	journal	December 2001
A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring Hatzenpichler, R.; Lebedeva, E. V.; Spieck, E. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0708857105	journal	February 2008
Respiration Response Imaging for Real-Time Detection of Microbial Function at the Single-Cell Level Konopka, M. C.; Strovas, T. J.; Ojala, David S. Applied and Environmental Microbiology, Vol. 77, Issue 1 https://doi.org/10.1128/AEM.01166-10	journal	November 2010
Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms Wallner, Günter; Amann, Rudolf; Beisker, Wolfgang Cytometry, Vol. 14, Issue 2 https://doi.org/10.1002/cyto.990140205	journal	January 1993
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
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus Kashtan, N.; Roggensack, S. E.; Rodrigue, S. Science, Vol. 344, Issue 6182 https://doi.org/10.1126/science.1248575	journal	April 2014
Methanogenic capabilities of ANME-archaea deduced from ¹³ C-labelling approaches : Methanogenesis of ANME Bertram, Sebastian; Blumenberg, Martin; Michaelis, Walter Environmental Microbiology, Vol. 15, Issue 8 https://doi.org/10.1111/1462-2920.12112	journal	March 2013
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
In situ visualization of newly synthesized proteins in environmental microbes using amino acid tagging and click chemistry : Visualizing new proteins in microbes by click chemistry Hatzenpichler, Roland; Scheller, Silvan; Tavormina, Patricia L. Environmental Microbiology, Vol. 16, Issue 8 https://doi.org/10.1111/1462-2920.12436	journal	April 2014
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
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
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
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Noncanonical Amino Acids in the Interrogation of Cellular Protein Synthesis Ngo, John T.; Tirrell, David A. Accounts of Chemical Research, Vol. 44, Issue 9 https://doi.org/10.1021/ar200144y	journal	September 2011
Distribution of the verrucomicrobial clade S partobacteria along a salinity gradient in the Baltic Sea : Quantifying Bergen, Benjamin; Herlemann, Daniel P. R.; Labrenz, Matthias Environmental Microbiology Reports, Vol. 6, Issue 6 https://doi.org/10.1111/1758-2229.12178	journal	June 2014
Reagent and laboratory contamination can critically impact sequence-based microbiome analyses Salter, Susannah J.; Cox, Michael J.; Turek, Elena M. BMC Biology, Vol. 12, Issue 1 https://doi.org/10.1186/s12915-014-0087-z	journal	November 2014
Methods for unveiling cryptic microbial partnerships in nature Orphan, Victoria J. Current Opinion in Microbiology, Vol. 12, Issue 3 https://doi.org/10.1016/j.mib.2009.04.003	journal	June 2009
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
Molecular biogeochemistry of sulfate reduction, methanogenesis and the anaerobic oxidation of methane at Gulf of Mexico cold seeps Orcutt, Beth!; Boetius, Antje; Elvert, Marcus Geochimica et Cosmochimica Acta, Vol. 69, Issue 17 https://doi.org/10.1016/j.gca.2005.04.012	journal	September 2005
Geobiological investigations using secondary ion mass spectrometry: microanalysis of extant and paleo-microbial processes Orphan, V. J.; House, C. H. Geobiology, Vol. 7, Issue 3 https://doi.org/10.1111/j.1472-4669.2009.00201.x	journal	June 2009
Selective Dye-Labeling of Newly Synthesized Proteins in Bacterial Cells Beatty, Kimberly E.; Xie, Fang; Wang, Qian Journal of the American Chemical Society, Vol. 127, Issue 41 https://doi.org/10.1021/ja054643w	journal	October 2005
Functional analysis of natural microbial consortia using community proteomics VerBerkmoes, Nathan C.; Denef, Vincent J.; Hettich, Robert L. Nature Reviews Microbiology, Vol. 7, Issue 3 https://doi.org/10.1038/nrmicro2080	journal	March 2009
Effects of sample treatments on genome recovery via single-cell genomics Clingenpeel, Scott; Schwientek, Patrick; Hugenholtz, Philip The ISME Journal, Vol. 8, Issue 12 https://doi.org/10.1038/ismej.2014.92	journal	June 2014
Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging Dieterich, Daniela C.; Lee, Jennifer J.; Link, A. James Nature Protocols, Vol. 2, Issue 3 https://doi.org/10.1038/nprot.2007.52	journal	March 2007
Development of a 16S rRNA-targeted probe set for Verrucomicrobia and its application for fluorescence in situ hybridization in a humic lake Arnds, Julia; Knittel, Katrin; Buck, Ulrike Systematic and Applied Microbiology, Vol. 33, Issue 3 https://doi.org/10.1016/j.syapm.2009.12.005	journal	April 2010
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
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
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
The Molecular Timeline of a Reviving Bacterial Spore Sinai, Lior; Rosenberg, Alex; Smith, Yoav Molecular Cell, Vol. 57, Issue 4 https://doi.org/10.1016/j.molcel.2014.12.019	journal	February 2015
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
The future is now: single-cell genomics of bacteria and archaea Blainey, Paul C. FEMS Microbiology Reviews, Vol. 37, Issue 3 https://doi.org/10.1111/1574-6976.12015	journal	May 2013
Oceanic Methane Biogeochemistry Reeburgh, William S. Chemical Reviews, Vol. 107, Issue 2 https://doi.org/10.1021/cr050362v	journal	February 2007
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
Single-Cell Ecophysiology of Microbes as Revealed by Raman Microspectroscopy or Secondary Ion Mass Spectrometry Imaging Wagner, Michael Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073233	journal	October 2009
In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area Nauhaus, Katja; Boetius, Antje; Kruger, Martin Environmental Microbiology, Vol. 4, Issue 5 https://doi.org/10.1046/j.1462-2920.2002.00299.x	journal	May 2002
Raman tweezers sorting of single microbial cells Huang, Wei E.; Ward, Andrew D.; Whiteley, Andrew S. Environmental Microbiology Reports, Vol. 1, Issue 1 https://doi.org/10.1111/j.1758-2229.2008.00002.x	journal	February 2009
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
Fluorescence Visualization of Newly Synthesized Proteins in Mammalian Cells Beatty, Kimberly E.; Liu, Julie C.; Xie, Fang Angewandte Chemie International Edition, Vol. 45, Issue 44 https://doi.org/10.1002/anie.200602114	journal	November 2006
Methyloprofundus sedimenti gen. nov., sp. nov., an obligate methanotroph from ocean sediment belonging to the 'deep sea-1' clade of marine methanotrophs Tavormina, P. L.; Hatzenpichler, R.; McGlynn, S. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 65, Issue Pt 1 https://doi.org/10.1099/ijs.0.062927-0	journal	October 2014
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
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
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
Reconstructing each cell's genome within complex microbial communitiesâ€”dream or reality? Clingenpeel, Scott; Clum, Alicia; Schwientek, Patrick Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00771	journal	January 2015
Quantitative, Time-Resolved Proteomic Analysis by Combining Bioorthogonal Noncanonical Amino Acid Tagging and Pulsed Stable Isotope Labeling by Amino Acids in Cell Culture Bagert, John D.; Xie, Yushu J.; Sweredoski, Michael J. Molecular & Cellular Proteomics, Vol. 13, Issue 5 https://doi.org/10.1074/mcp.M113.031914	journal	February 2014
Consumption of Methane and CO2 by Methanotrophic Microbial Mats from Gas Seeps of the Anoxic Black Sea Treude, T.; Orphan, V.; Knittel, K. Applied and Environmental Microbiology, Vol. 73, Issue 7 https://doi.org/10.1128/AEM.02685-06	journal	February 2007
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
Growth and activity of ANME clades with different sulfate and sulfide concentrations in the presence of methane Timmers, Peer H. A.; Widjaja-Greefkes, H. C. A.; Ramiro-Garcia, Javier Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00988	journal	September 2015
Two-color labeling of temporally defined protein populations in mammalian cells Beatty, Kimberly E.; Tirrell, David A. Bioorganic & Medicinal Chemistry Letters, Vol. 18, Issue 22 https://doi.org/10.1016/j.bmcl.2008.08.046	journal	November 2008
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
Tracking heavy water (D ₂ O) incorporation for identifying and sorting active microbial cells Berry, David; Mader, Esther; Lee, Tae Kwon Proceedings of the National Academy of Sciences, Vol. 112, Issue 2 https://doi.org/10.1073/pnas.1420406112	journal	December 2014
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
Who eats what, where and when? Isotope-labelling experiments are coming of age Neufeld, Josh D.; Wagner, Michael; Murrell, J. Colin The ISME Journal, Vol. 1, Issue 2 https://doi.org/10.1038/ismej.2007.30	journal	May 2007
Extensive carbon isotopic heterogeneity among methane seep microbiota House, Christopher H.; Orphan, Victoria J.; Turk, Kendra A. Environmental Microbiology, Vol. 11, Issue 9 https://doi.org/10.1111/j.1462-2920.2009.01934.x	journal	September 2009
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
Individual cell DNA synthesis within natural marine bacterial assemblages as detected by ‘click’ chemistry Smriga, S.; Samo, Tj; Malfatti, F. Aquatic Microbial Ecology, Vol. 72, Issue 3 https://doi.org/10.3354/ame01698	journal	July 2014
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
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics Rinke, Christian; Lee, Janey; Nath, Nandita Nature Protocols, Vol. 9, Issue 5 https://doi.org/10.1038/nprot.2014.067	journal	April 2014
Zero-valent sulphur is a key intermediate in marine methane oxidation Milucka, Jana; Ferdelman, Timothy G.; Polerecky, Lubos Nature, Vol. 491, Issue 7425 https://doi.org/10.1038/nature11656	journal	November 2012
The Domain-specific Probe EUB338 is Insufficient for the Detection of all Bacteria: Development and Evaluation of a more Comprehensive Probe Set Daims, Holger; Brühl, Andreas; Amann, Rudolf Systematic and Applied Microbiology, Vol. 22, Issue 3 https://doi.org/10.1016/S0723-2020(99)80053-8	journal	September 1999
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
Phylogenetic Oligodeoxynucleotide Probes for the Major Subclasses of Proteobacteria: Problems and Solutions Manz, Werner; Amann, Rudolf; Ludwig, Wolfgang Systematic and Applied Microbiology, Vol. 15, Issue 4 https://doi.org/10.1016/S0723-2020(11)80121-9	journal	December 1992
Niche Separation of Methanotrophic Archaea (ANME-1 and -2) in Methane-Seep Sediments of the Eastern Japan Sea Offshore Joetsu Yanagawa, Katsunori; Sunamura, Michinari; Lever, Mark Alexander Geomicrobiology Journal, Vol. 28, Issue 2 https://doi.org/10.1080/01490451003709334	journal	February 2011
Environmental evidence for net methane production and oxidation in putative ANaerobic MEthanotrophic (ANME) archaea: Methanogenesis and methanotrophy in ANME-1 archaea Lloyd, Karen G.; Alperin, Marc J.; Teske, Andreas Environmental Microbiology, Vol. 13, Issue 9 https://doi.org/10.1111/j.1462-2920.2011.02526.x	journal	August 2011
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
In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons Dieterich, Daniela C.; Hodas, Jennifer J. L.; Gouzer, Géraldine Nature Neuroscience, Vol. 13, Issue 7 https://doi.org/10.1038/nn.2580	journal	June 2010
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Global distribution and diversity of marine Verrucomicrobia Freitas, Sara; Hatosy, Stephen; Fuhrman, Jed A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.3	journal	February 2012
Immunological Localization of Coenzyme M Reductase in Anaerobic Methane-Oxidizing Archaea of ANME 1 and ANME 2 Type Heller, Christina; Hoppert, Michael; Reitner, Joachim Geomicrobiology Journal, Vol. 25, Issue 3-4 https://doi.org/10.1080/01490450802006884	journal	June 2008
probeCheck - a central resource for evaluating oligonucleotide probe coverage and specificity: probeCheck - an online probe match tool Loy, Alexander; Arnold, Roland; Tischler, Patrick Environmental Microbiology, Vol. 10, Issue 10 https://doi.org/10.1111/j.1462-2920.2008.01706.x	journal	July 2008
Sizing up metatranscriptomics Moran, Mary Ann; Satinsky, Brandon; Gifford, Scott M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.94	journal	August 2012
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
Improved 16S rRNA-targeted probe set for analysis of sulfate-reducing bacteria by fluorescence in situ hybridization Lücker, Sebastian; Steger, Doris; Kjeldsen, Kasper Urup Journal of Microbiological Methods, Vol. 69, Issue 3 https://doi.org/10.1016/j.mimet.2007.02.009	journal	June 2007
Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT) Dieterich, D. C.; Link, A. J.; Graumann, J. Proceedings of the National Academy of Sciences, Vol. 103, Issue 25 https://doi.org/10.1073/pnas.0601637103	journal	June 2006
Fixation-free fluorescence in situ hybridization for targeted enrichment of microbial populations Yilmaz, Suzan; Haroon, Mohamed F.; Rabkin, Brian A. The ISME Journal, Vol. 4, Issue 10 https://doi.org/10.1038/ismej.2010.73	journal	May 2010
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
Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities Nauhaus, Katja; Treude, Tina; Boetius, Antje Environmental Microbiology, Vol. 7, Issue 1 https://doi.org/10.1111/j.1462-2920.2004.00669.x	journal	January 2005

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Title: Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

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