Characterization of microbial associations with methanotrophic archaea and sulfate-reducing bacteria through statistical comparison of nested Magneto-FISH enrichments

PeerJ

Volumn 2016, Issue 4, 2016, Pages

  Trembath Reichert, Elizabeth ^a   Case, David H ^a   Orphan, Victoria J ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Anaerobic oxidation of methane; Co occurrence network; Earth microbiome project; ITag sequencing; Magneto FISH; Microbial association; Microbial ecology

Indexed keywords

DNA; METHANE; RNA 16S;

ANAEROBIC METABOLISM; ARTICLE; ATRIBACTERIA; BIOINFORMATICS; CHEMOTAXONOMY; COMMUNITY STRUCTURE; CONTROLLED STUDY; DELTAPROTEOBACTERIA; EPSILONPROTEOBACTERIA; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMAPROTEOBACTERIA; GENE LIBRARY; MARINE BIOLOGY; METHANOTROPHIC BACTERIUM; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; POLYMERASE CHAIN REACTION; SULFATE REDUCING BACTERIUM;

EID: 84966429168     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.1913     Document Type: Article

References (83)

1. Akerman NH, Butterfield DA, Huber JA. 2013. Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Frontiers in Microbiology 4:185 DOI 10.3389/fmicb.2013.00185.
2. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Applied and Environmental Microbiology 56:1919-1925.
3. Ashkin A. 1997. Optical trapping and manipulation of neutral particles using lasers. Proceedings of the National Academy of Sciences of the United States of America 94:4853-4860 DOI 10.1073/pnas.94.10.4853.
4. Barberán A, Bates ST, Casamayor EO, Fierer N. 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. The ISME Journal 6:343-351 DOI 10.1038/ismej.2011.119.
5. Berry D, Mader E, Lee TK, Woebken D, Wang Y, Zhu D, Palatinszky M, Schintlmeister A, Schmid MC, Hanson BT, Shterzer N, Mizrahi I, Rauch I, Decker T, Bocklitz T, Popp Jr, Gibson CM, Fowler PW, Huang WE, Wagner M. 2015. Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. Proceedings of the National Academy of Sciences of the United States of America 112:E194-E203 DOI 10.1073/pnas.1420406112.
6. Blazejak A, Kuever J, Erséus JL, Amann R, Dubilier N. 2006. Phylogeny of 16S rRNA, ribulose 1, 5-bisphosphate carboxylase/oxygenase, and adenosine 50-phosphosulfate reductase genes from gamma-and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from bermuda and the bahamas. Applied and Environmental Microbiology 72:5527-5536 DOI 10.1128/aem.02441-05.
7. Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jorgensen BB, Witte U, Pfannkuche O. 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623-626 DOI 10.1038/35036572.
8. Campbell BJ, Engel AS, Porter ML, Takai K. 2006. The versatile [epsi]-proteobacteria: key players in sulphidic habitats. Nature Reviews Microbiology 4:458-468 DOI 10.1038/nrmicro1414.
9. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. 2012. Ultrahigh-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6:1621-1624 DOI 10.1038/ismej.2012.8.
10. Chaffron S, Rehrauer H, Pernthaler J, Von Mering C. 2010. A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Research 20:947-959 DOI 10.1101/gr.104521.109.
11. Chandler DP, Fredrickson JK, Brockman FJ. 1997. Effect of PCR template concentration on the composition and distribution of total community 16S rDNA clone libraries. Molecular Ecology 6:475-482 DOI 10.1046/j.1365-294X.1997.00205.x.
12. DeLong EF. 1992. Archaea in coastal marine environments. Proceedings of the National Academy of Sciences of the United States of America 89:5685-5689.
13. Dubinina GA, Grabovich MY, Chernyshova YY. 2004. The role of oxygen in the regulation of the metabolism of aerotolerant spirochetes, a major component of "Thiodendron" bacterial sulfur mats. Microbiology 73:621-628 DOI 10.1007/s11021-005-0001-3.
14. Duperron S, Rodrigues CF, Léger N, Szafranski K, Decker C, Olu K, Gaudron SM. 2012. Diversity of symbioses between chemosynthetic bacteria and metazoans at the Guiness cold seep site (Gulf of Guinea, West Africa). Microbiology Open 1:467-480 DOI 10.1002/mbo3.47.
15. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194-2200 DOI 10.1093/bioinformatics/btr381.
16. Friedman J, Alm EJ. 2012. Inferring correlation networks from genomic survey data. PLoS Computational Biology 8:e1002687.
17. Fuseler K, Cypionka H. 1995. Elemental sulfur as an intermediate of sulfide oxidation with oxygen by Desulfobulbus propionicus. Archives of Microbiology 164:104-109 DOI 10.1007/BF02525315.
18. Goffredi SK. 2010. Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates. Environmental Microbiology Reports 2:479-488 DOI 10.1111/j.1758-2229.2010.00136.x.
19. Green-Saxena A, Dekas AE, Dalleska NF, Orphan VJ. 2014. Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. The ISME Journal 8:150-163 DOI 10.1038/ismej.2013.147.
20. Greuter D, Loy A, Horn M, Rattei T. 2016. probeBase-an online resource for rRNAtargeted oligonucleotide probes and primers: new features 2016. Nucleic Acids Research 44:D586-D589 DOI 10.1093/nar/gkv1232.
21. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59:307-321 DOI 10.1093/sysbio/syq010.
22. Hatzenpichler R, Orphan V. 2015. Detection of protein-synthesizing microorganisms in the environment via bioorthogonal noncanonical amino acid tagging (BONCAT). Totowa: Humana Press, 1-13.
23. Hatzenpichler R, Scheller S, Tavormina PL, Babin BM, Tirrell DA, Orphan VJ. 2014. In situ visualization of newly synthesized proteins in environmental microbes using amino acid tagging and click chemistry. Environmental Microbiology 16:2568-2590 DOI 10.1111/1462-2920.12436.
24. House CH, Orphan VJ, Turk KA, Thomas B, Pernthaler A, Vrentas JM, Joye SB. 2009. Extensive carbon isotopic heterogeneity among methane seep microbiota. Environmental Microbiology 11:2207-2215 DOI 10.1111/j.1462-2920.2009.01934.x.
25. Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, Suzuki M, Takai K, Delwiche M, Colwell FS, Nealson KH, Horikoshi K, D'Hondt S, Jørgensen BB. 2006. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proceedings of the National Academy of Sciences of the United States of America 103:2815-2820 DOI 10.1073/pnas.0511033103.
26. Inagaki F, Takai K, Kobayashi H, Nealson KH, Horikoshi K. 2003. Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing×m-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. International Journal of Systematic and Evolutionary Microbiology 53:1801-1805 DOI 10.1099/ijs.0.02682-0.
27. Inagaki F, Takai K, Nealson KH, Horikoshi K. 2004. Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the ×m-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. International Journal of Systematic and Evolutionary Microbiology 54:1477-1482 DOI 10.1099/ijs.0.03042-0.
28. Kalyuzhnaya M, Lidstrom M, Chistoserdova L. 2008. Real-time detection of actively metabolizing microbes by redox sensing as applied to methylotroph populations in Lake Washington. The ISME Journal 2:696-706 DOI 10.1038/ismej.2008.32.
29. Knittel K, Boetius A, Lemke A, Eilers H, Lochte K, Pfannkuche O, Linke P, Amann R. 2003. Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia Margin, Oregon). Geomicrobiology Journal 20:269-294 DOI 10.1080/01490450303896.
30. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Applied and Environmental Microbiology 79:5112-5120 DOI 10.1128/AEM.01043-13.
31. Lane DJ. 1991. 16S/23S rRNA sequencing. In: Stackebrandt EaG M, ed. Nucleic acid techniques in bacterial systematics. Chichester: John Wiley & Sons, 115-175.
32. Lenk S, Arnds J, Zerjatke K, Musat N, Amann R, Mussmann M. 2011. Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment. Environmental Microbiology 13:758-774 DOI 10.1111/j.1462-2920.2010.02380.x.
33. Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, Park YM, Buso N, Lopez R. 2015. The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Research Epub ahead of print April 6 2015 DOI 10.1093/nar/gkv279.
34. Löesekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A, Amann R. 2007. Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Applied and Environmental Microbiology 73:3348-3362 DOI 10.1128/AEM.00016-07.
35. Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J, Schleifer K-H, Wagner M. 2002. Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Applied and Environmental Microbiology 68:5064-5081 DOI 10.1128/aem.68.10.5064-5081.2002.
36. Lozupone C, Knight R. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71:8228-8235 DOI 10.1128/AEM.71.12.8228-8235.2005.
37. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüÿmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H. 2004. ARB: a software environment for sequence data. Nucleic Acids Research 32:1363-1371 DOI 10.1093/nar/gkh293.
38. Macalady JL, Dattagupta S, Schaperdoth I, Jones DS, Druschel GK, Eastman D. 2008. Niche differentiation among sulfur-oxidizing bacterial populations in cave waters. The ISME Journal 2:590-601 DOI 10.1038/ismej.2008.25.
39. Macalady JL, Lyon EH, Koffman B, Albertson LK, Meyer K, Galdenzi S, Mariani S, Wagner M. 2006. Dominant microbial populations in limestone-corroding stream biofilms, frasassi cave system, Italy. Applied and Environmental Microbiology 72:5596-5609 DOI 10.1128/aem.00715-06.
40. Malfatti F, Azam F. 2010. Atomic force microscopy reveals microscale networks and possible symbioses among pelagic marine bacteria. Aquatic Microbial Ecology 58:1-14 DOI 10.3354/ame01355.
41. Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer K-H. 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142:1097-1106 DOI 10.1099/13500872-142-5-1097.
42. Manz W, Amann R, Ludwig W, Wagner M, Schleifer KH. 1992. Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria-problems and solutions. Systematic and Applied Microbiology 15:593-600.
43. Manz W, Eisenbrecher M, Neu TR, Szewzyk U. 1998. Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides. FEMS Microbiology Ecology 25:43-61 DOI 10.1111/j.1574-6941.1998.tb00459.x.
44. McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ. 2015. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526:531-535 DOI 10.1038/nature15512.
45. Melin J, Quake SR. 2007. Microfluidic large-scale integration: the evolution of design rules for biological automation. Annual Review of Biophysics and Biomolecular Structure 36:213-231 DOI 10.1146/annurev.biophys.36.040306.132646.
46. 2 injection. Frontiers in Microbiology 6:263 DOI 10.3389/fmicb.2015.00263.
47. Neef A, Amann R, Schlesner H, Schleifer K-H. 1998. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbi-ology 144:3257-3266 DOI 10.1099/00221287-144-12-3257.
48. Niemann H, Loesekann T, De Beer D, Elvert M, Nadalig T, Knittel K, Amann R, Sauter EJ, Schluter M, Klages. 2006. Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature 443:854-858 DOI 10.1038/nature05227.
49. Nobu MK, Dodsworth JA, Murugapiran SK, Rinke C, Gies EA, Webster G, Schwientek P, Kille P, Parkes RJ, Sass H, Jorgensen BB, Weightman AJ, Liu W-T, Hallam SJ, Tsiamis G, Woyke T, Hedlund BP. 2016. Phylogeny and physiology of candidate phylum 'Atribacteria' (OP9/JS1) inferred from cultivation-independent genomics. The ISME Journal 10:273-286 DOI 10.1038/ismej.2015.97.
50. Omoregie EO, Mastalerz V, De Lange G, Straub KL, Kappler A, Røy H, Stadnitskaia A, Foucher J-P, Boetius A. 2008. Biogeochemistry and community composition of iron-and sulfur-precipitating microbial mats at the Chefren Mud Volcano (Nile Deep Sea Fan, Eastern Mediterranean). Applied and Environmental Microbiology 74:3198-3215 DOI 10.1128/AEM.01751-07.
51. Orphan VJ. 2009. Methods for unveiling cryptic microbial partnerships in nature. Current Opinion in Microbiology 12:231-237 DOI 10.1016/j.mib.2009.04.003.
52. Orphan VJ, Hinrichs KU, Ussler W, Paull CK, Taylor LT, Sylva SP, Hayes JM, Delong EF. 2001a. Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Applied and Environmental Microbiology 67:1922-1934 DOI 10.1128/AEM.67.4.1922-1934.2001.
53. Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF. 2001b. Methaneconsuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293:484-487 DOI 10.1126/science.1061338.
54. Orphan VJ, House CH, Hinrichs KU, McKeegan KD, DeLong EF. 2002. Direct phylogenetic and isotopic evidence for multiple groups of archaea involved in the anaerobic oxidation of methane. Geochimica Et Cosmochimica Acta 66:A571-A571.
55. Parada A, Needham DM, Fuhrman JA. 2015. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time-series and global field samples. Environmental Microbiology n/a-n/a DOI 10.1111/1462-2920.13023.
56. Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ. 2008. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proceedings of the National Academy of Sciences of the United States of America 105:7052-7057 DOI 10.1073/pnas.0711303105.
57. Pjevac P, Kamyshny A, Dyksma S, Muÿmann M. 2014. Microbial consumption of zero-valence sulfur in marine benthic habitats. Environmental Microbiology 16:3416-3430 DOI 10.1111/1462-2920.12410.
58. Pruesse E, Peplies J, Glöckner FO. 2012. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823-1829 DOI 10.1093/bioinformatics/bts252.
59. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41:D590-D596 DOI 10.1093/nar/gks1219.
60. R Core Team. 2015. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at http://www.R-project.org/.
61. Ravenschlag K, Sahm K, Pernthaler J, Amann R. 1999. High bacterial diversity in permanently cold marine sediments. Applied and Environmental Microbiology 65:3982-3989.
62. Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A. 2015. Global dispersion and local diversification of the methane seep microbiome. Proceedings of the National Academy of Sciences of the United States of America 112:4015-4020 DOI 10.1073/pnas.1421865112.
63. Safařík I, Safaříková M. 1999. Use of magnetic techniques for the isolation of cells. Journal of Chromatography B 722:33-53 DOI 10.1016/S0378-4347(98)00338-7.
64. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW. 2014. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biology 12:87 DOI 10.1186/s12915-014-0087-z.
65. Schattenhofer M, Wendeberg A. 2011. Capturing microbial populations for environmental genomics. In: Bruijn FJd, ed. Handbook of molecular microbial ecology I: metagenomics and complementary approaches. Hoboken: John Wiley & Sons, Inc., 735-740.
66. Schreiber L, Holler T, Knittel K, Meyerdierks A, Amann R. 2010. Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade. Environmental Microbiology 12:2327-2340 DOI 10.1111/j.14622920.2010.02275.x.
67. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology 12:1-18 DOI 10.1186/gb-2011-12-6-r60.
68. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13:2498-2504 DOI 10.1101/gr.1239303.
69. Sorokin DY, Kovaleva OL, Tourova TP, Muyzer G. 2010. Thiohalobacter thiocyanaticus gen. nov., sp. nov., a moderately halophilic, sulfur-oxidizing gammaproteobacterium from hypersaline lakes, that utilizes thiocyanate. International Journal of Systematic and Evolutionary Microbiology 60:444-450 DOI 10.1099/ijs.0.012880-0.
70. Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, Chow C-ET, Sachdeva R, Jones AC, Schwalbach MS, Rose JM, Hewson I, Patel A, Sun F, Caron DA, Fuhrman JA. 2011. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. The ISME Journal 5:1414-1425 DOI 10.1038/ismej.2011.24.
71. Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, Djahanschiri B, Zeller G, Mende DR, Alberti A, Cornejo-Castillo FM, Costea PI, Cruaud C, D'Ovidio F, Engelen S, Ferrera I, Gasol JM, Guidi L, Hildebrand F, Kokoszka F, Lepoivre C, Lima-Mendez G, Poulain J, Poulos BT, Royo-Llonch M, Sarmento H, Vieira-Silva S, Dimier CI, Picheral M, Searson S, Kandels-Lewis S, Bowler C, De Vargas C, Gorsky G, Grimsley N, Hingamp P, Iudicone D, Jaillon O, Not F, Ogata H, Pesant S, Speich S, Stemmann L, Sullivan MB, Weissenbach J, Wincker P, Karsenti E, Raes J, Acinas SG, Bork P, Boss E, Follows M, Karp-Boss L, Krzic U, Reynaud EG, Sardet C, Sieracki M, Velayoudon D. 2015. Structure and function of the global ocean microbiome. Science 348:1-9 DOI 10.1126/science.1261359.
72. Takano Y, Kaneko M, Kahnt J, Imachi H, Shima S, Ohkouchi N. 2013. Detection of coenzyme F430 in deep sea sediments: a key molecule for biological methanogenesis. Organic Geochemistry 58:137-140 DOI 10.1016/j.orggeochem.2013.01.012.
73. Trembath-Reichert E, Green-Saxena A, Orphan VJ. 2013. Chapter two-whole cell immunomagnetic enrichment of environmental microbial consortia using rRNATargeted Magneto-FISH. In: Edward FD, ed. Microbial metagenomics, metatranscrip-tomics, and metaproteomics. San Diego: Academic Press, 21-44.
74. 2 by methanotrophic microbial mats from gas seeps of the Anoxic Black Sea. Applied and Environmental Microbiology 73:2271-2283 DOI 10.1128/AEM.02685-06.
75. Vigneron A, L'Haridon SP, Godfroy A, Roussel EG, Cragg BA, Parkes RJ, Toffin L. 2015. Evidence of active methanogen communities in shallow sediments of the sonora margin cold seeps. Applied and Environmental Microbiology 81:3451-3459 DOI 10.1128/AEM.00147-15.
76. Von Wintzingerode F, Selent B, Hegemann W, Göbel UB. 1999. Phylogenetic analysis of an anaerobic, trichlorobenzene-transforming microbial consortium. Applied and Environmental Microbiology 65:283-286.
77. Wagner M, Roger AJ, Flax JL, Brusseau GA, Stahl DA. 1998. Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. Journal of Bacteriol-ogy 180:2975-2982.
78. Wegener G, Bausch M, Holler T, Thang NM, Prieto Mollar X, Kellermann MY, Hinrichs K-U, Boetius A. 2012. Assessing sub-seafloor microbial activity by combined stable isotope probing with deuterated water and 13C-bicarbonate. Environmental Microbiology 14:1517-1527 DOI 10.1111/j.1462-2920.2012.02739.x.
79. Wegener G, Krukenberg V, Riedel D, Tegetmeyer HE, Boetius A. 2015. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526:587-590 DOI 10.1038/nature15733.
80. White JR, Nagarajan N, Pop M. 2009. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Computational Biology 5:e1000352 DOI 10.1371/journal.pcbi.1000352.
81. Wright JJ, Mewis K, Hanson NW, Konwar KM, Maas KR, Hallam SJ. 2014. Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle. The ISME Journal 8:455-468 DOI 10.1038/ismej.2013.152.
82. Yanagawa K, Sunamura M, Lever MA, Morono Y, Hiruta A, Ishizaki O, Matsumoto R, Urabe T, Inagaki F. 2011. Niche separation of methanotrophic archaea (ANME-1 and-2) in methane-seep sediments of the eastern Japan Sea offshore Joetsu. Geomicrobiology Journal 28:118-129 DOI 10.1080/01490451003709334.
83. Yilmaz S, Haroon MF, Rabkin BA, Tyson GW, Hugenholtz P. 2010. Fixation-free fluorescence in situ hybridization for targeted enrichment of microbial populations. The ISME Journal 4:1352-1356 DOI 10.1038/ismej.2010.73.