Skip to main content
SpringerLink
Log in

Anaerobic Methane-Oxidizing Microbial Community in a Coastal Marine Sediment: Anaerobic Methanotrophy Dominated by ANME-3

Microbial Ecology volume 74, pages 608–622 (2017)Cite this article

Abstract

The microbial community inhabiting the shallow sulfate-methane transition zone in coastal sediments from marine Lake Grevelingen (The Netherlands) was characterized, and the ability of the microorganisms to carry out anaerobic oxidation of methane coupled to sulfate reduction was assessed in activity tests. In vitro activity tests of the sediment with methane and sulfate demonstrated sulfide production coupled to the simultaneous consumption of sulfate and methane at approximately equimolar ratios over a period of 150 days. The maximum sulfate reduction rate was 5 μmol sulfate per gram dry weight per day during the incubation period. Diverse archaeal and bacterial clades were retrieved from the sediment with the majority of them clustered with Euryarchaeota, Thaumarcheota, Bacteroidetes, and Proteobacteria. The 16S rRNA gene sequence analysis showed that the sediment from marine Lake Grevelingen contained anaerobic methanotrophic Archaea (ANME) and methanogens as archaeal clades with a role in the methane cycling. ANME at the studied site mainly belong to the ANME-3 clade. This study provides one of the few reports for the presence of ANME-3 in a shallow coastal sediment. Sulfate-reducing bacteria from Desulfobulbus clades were found among the sulfate reducers, however, with very low relative abundance. Desulfobulbus has previously been commonly found associated with ANME, whereas in our study, ANME-3 and Desulfobulbus were not observed simultaneously in clusters, suggesting the possibility of independent AOM by ANME-3.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem. Rev. 107:486–513. doi:10.1021/cr050362v

    Article  CAS  PubMed  Google Scholar 

  2. Tavormina PL, Ussler W, Joye SB, Harrison BK, Orphan VJ (2010) Distributions of putative aerobic methanotrophs in diverse pelagic marine environments. ISME J 4:700–710. doi:10.1038/ismej.2009.155

    Article  PubMed  Google Scholar 

  3. Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63:311–334. doi:10.1146/annurev.micro.61.080706.093130

    Article  CAS  PubMed  Google Scholar 

  4. Wankel SD, Adams MM, Johnston DT, Hansel CM, Joye SB, Girguis PR (2012) Anaerobic methane oxidation in metalliferous hydrothermal sediments: influence on carbon flux and decoupling from sulfate reduction. Environ. Microbiol. 14:2726–2740. doi:10.1111/j.1462-2920.2012.02825.x

    Article  CAS  PubMed  Google Scholar 

  5. Ruff SE, Kuhfuss H, Wegener G, Lott C, Ramette A, Wiedling J, Knittel K, Weber M (2016) Methane seep in shallow-water permeable sediment harbors high diversity of anaerobic methanotrophic communities, Elba, Italy. Front. Microbiol. 7:374. doi:10.3389/fmicb.2016.00374

    Article  PubMed  PubMed Central  Google Scholar 

  6. Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jørgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626. doi:10.1038/35036572

    Article  CAS  PubMed  Google Scholar 

  7. Hinrichs KU, Hayes JM, Sylva SP, Brewer PG, DeLong EF (1999) Methane-consuming archaebacteria in marine sediments. Nature 398:802–805. doi:10.1007/s00248-006-9172-3

    Article  CAS  PubMed  Google Scholar 

  8. Hoehler TM, Alperin MJ, Albert DB, Martens S (1994) Field and laboratory studies of methane oxidation in an anoxic marine sediment: evidence for a methanogen-sulfate reducer consortium. Global Biogeochem Cy 8:451–463. doi:10.1029/94GB01800

    Article  CAS  Google Scholar 

  9. Meulepas RJW, Jagersma CG, Gieteling J, Buisman CJN, Stams AJM, Lens PNL (2009) Enrichment of anaerobic methanotrophs in sulfate-reducing membrane bioreactors. Biotechnol. Bioeng. 104:458–470. doi:10.1002/bit.22412

    Article  CAS  PubMed  Google Scholar 

  10. Nauhaus K, Boetius A, Krüger M, Widdel F (2002) In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ. Microbiol. 4:296–305. doi:10.1046/j.1462-2920.2002.00299.x

    Article  CAS  PubMed  Google Scholar 

  11. Niemann H, Duarte J, Hensen C, Omoregie E, Magalhaes VH, Elvert M, Pinheiro LM, Kopf A, Boetius A (2006) Microbial methane turnover at mud volcanoes of the Gulf of Cadiz. Geochim Cosmochim Ac 70:5336–5355. doi:10.1016/j.gca.2006.08.010

    Article  CAS  Google Scholar 

  12. Beal EJ, House CH, Orphan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325:184–187. doi:10.1126/science.1169984

    Article  CAS  PubMed  Google Scholar 

  13. Egger M, Rasigraf O, Sapart CJ, Jilbert T, Jetten MS, Röckmann T, van der Veen C, Bândă N, Kartal B, Ettwig KF (2015) Iron-mediated anaerobic oxidation of methane in brackish coastal sediments. Environ Sci Technol 49:277–283. doi:10.1021/es503663z

    Article  CAS  PubMed  Google Scholar 

  14. Ettwig KF, Zhu B, Speth D, Keltjens JT, Jetten MS, Kartal B (2016) Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc. Natl. Acad. Sci. U. S. A. 113:12792–12796. doi:10.1073/pnas.1609534113

    Article  CAS  PubMed Central  Google Scholar 

  15. Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ (2016) Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351:703–707. doi:10.1126/science.aad7154

    Article  CAS  PubMed  Google Scholar 

  16. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJCT, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJM, Janssen-Megens EM, Francoijs K-J, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548. doi:10.1038/nature08883

    Article  CAS  PubMed  Google Scholar 

  17. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan Z, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570. doi:10.1038/nature12375

    Article  CAS  PubMed  Google Scholar 

  18. Arshad A, Speth DR, de Graaf RM, Op den Camp HJM, Jetten MSM, Welte CU (2015) A metagenomics-based metabolic model of nitrate-dependent anaerobic oxidation of methane by Methanoperedens-like archaea. Front. Microbiol. 6:1423. doi:10.3389/fmicb.2015.01423

    Article  PubMed  PubMed Central  Google Scholar 

  19. Milucka J, Ferdelman TG, Polerecky L, Franzke D, Wegener G, Schmid M, Lieberwirth I, Wagner M, Widdel F, Kuypers MMM (2012) Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491:541–546. doi:10.1038/nature11656

    Article  CAS  PubMed  Google Scholar 

  20. Knittel K, Lösekann T, Boetius A, Kort R, Amann R (2005) Diversity and distribution of methanotrophic archaea at cold seeps. Appl. Environ. Microbiol. 71:467–479. doi:10.1128/AEM.71.1.467-479.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sivan O, Schrag DP, Murray RW (2007) Rates of methanogenesis and methanotrophy in deep-sea sediments. Geobiology 5:141–151. doi:10.1111/j.1472-4669.2007.00098.x

    Article  CAS  Google Scholar 

  22. Blumenberg M, Seifert R, Reitner J, Pape T, Michaelis W (2004) Membrane lipid patterns typify distinct anaerobic methanotrophic consortia. Proc. Natl. Acad. Sci. U. S. A. 101:11111–11116. doi:10.1073/pnas.0401188101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Meyerdierks A, Kube M, Kostadinov I, Teeling H, Glöckner FO, Reinhardt R, Amann R (2010) Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. Environ. Microbiol. 12:422–439. doi:10.1111/j.1462-2920.2009.02083.x

    Article  CAS  PubMed  Google Scholar 

  24. Hinrichs KU, Summons RE, Orphan V, Sylva SP, Hayes JM (2000) Molecular and isotopic analysis of anaerobic methane-oxidizing communities in marine sediments. Org. Geochem. 31:1685–1701. doi:10.1007/s00248-006-9172-3

    Article  CAS  Google Scholar 

  25. Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF (2002) Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl. Acad. Sci. U. S. A. 99:7663–7668. doi:10.1073/pnas.072210299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Vigneron A, Cruaud P, Pignet P, Caprais J-C, Cambon-Bonavita M-A, Godfroy A, Toffin L (2013) Archaeal and anaerobic methane oxidizer communities in the Sonora Margin cold seeps, Guaymas Basin (Gulf of California). ISME J 7:1596–1608. doi:10.1038/ismej.2013.18

    Article  Google Scholar 

  27. Losekann 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. Appl. Environ. Microbiol. 73:3348–3362. doi:10.1128/aem.00016-07

    Article  PubMed  PubMed Central  Google Scholar 

  28. Niemann H, Losekann T, de Beer D, Elvert M, Nadalig T, Knittel K, Amann R, Sauter EJ, Schluter M, Klages M, Foucher JP, Boetius A (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

    Article  CAS  PubMed  Google Scholar 

  29. Boetius A, Wenzhofer F (2013) Seafloor oxygen consumption fuelled by methane from cold seeps. Nat. Geosci. 6:725–734. doi:10.1038/ngeo1926

    Article  CAS  Google Scholar 

  30. Orphan VJ, Ussler W, Naehr TH, House CH, Hinrichs KU, Paull CK (2004) Geological, geochemical, and microbiological heterogeneity of the seafloor around methane vents in the Eel River Basin, offshore California. Chem. Geol. 205:265–289. doi:10.1016/j.chemgeo.2003.12.035

    Article  CAS  Google Scholar 

  31. Biddle JF, Cardman Z, Mendlovitz H, Albert DB, Lloyd KG, Boetius A, Teske A (2011) Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments. ISME J 6:1018–1031. doi:10.1038/ismej.2011.164

    Article  PubMed  PubMed Central  Google Scholar 

  32. Brazelton WJ, Schrenk MO, Kelley DS, Baross JA (2006) Methane- and sulfur-metabolizing microbial communities dominate the lost City hydrothermal field ecosystem. Appl. Environ. Microbiol. 72:6257–6270. doi:10.1128/aem.00574-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Segarra KE, Comerford C, Slaughter J, Joye SB (2013) Impact of electron acceptor availability on the anaerobic oxidation of methane in coastal freshwater and brackish wetland sediments. Geochim Cosmochim Ac 115:15–30. doi:10.1016/j.gca.2013.03.029

    Article  CAS  Google Scholar 

  34. Segarra KEA, Schubotz F, Samarkin V, Yoshinaga MY, Hinrichs KU, Joye SB (2015) High rates of anaerobic methane oxidation in freshwater wetlands reduce potential atmospheric methane emissions. Nat Commun 6. doi:10.1038/ncomms8477

  35. Timmers PH, Suarez-Zuluaga DA, van Rossem M, Diender M, Stams AJ, Plugge CM (2015) Anaerobic oxidation of methane associated with sulfate reduction in a natural freshwater gas source. ISME J 10:12. doi:10.1038/ismej.2015.213

    Google Scholar 

  36. Holler T, Widdel F, Knittel K, Amann R, Kellermann MY, Hinrichs K-U, Teske A, Boetius A, Wegener G (2011) Thermophilic anaerobic oxidation of methane by marine microbial consortia. ISME J 5:1946–1956. doi:10.1038/ismej.2011.77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Orphan VJ, Hinrichs KU, Ussler W, Paull CK, Taylor LT, Sylva SP, Hayes JM, Delong EF (2001) Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl. Environ. Microbiol. 67:1922–1934. doi:10.1128/AEM.67.4.1922-1934.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Parkes RJ, Cragg BA, Banning N, Brock F, Webster G, Fry JC, Hornibrook E, Pancost RD, Kelly S, Knab N, Jørgensen BB, Rinna J, Weightman AJ (2007) Biogeochemistry and biodiversity of methane cycling in subsurface marine sediments (Skagerrak, Denmark). Environ. Microbiol. 9:1146–1161. doi:10.1111/j.1462-2920.2006.01237.x

    Article  CAS  PubMed  Google Scholar 

  39. Treude T, Krüger M, Boetius A, Jørgensen BB (2005) Environmental control on anaerobic oxidation of methane in the gassy sediments of Eckernförde Bay (German Baltic). Limnol. Oceanogr. 50:1771–1786. doi:10.4319/lo.2005.50.6.1771

    Article  CAS  Google Scholar 

  40. Oni OE, Miyatake T, Kasten S, Richter-Heitmann T, Fischer D, Wagenknecht L, Ksenofontov V, Kulkarni A, Blumers M, Shylin S (2015) Distinct microbial populations are tightly linked to the profile of dissolved iron in the methanic sediments of the Helgoland mud area, North Sea. Front. Microbiol. 6:365. doi:10.3389/fmicb.2015.00365

    PubMed  PubMed Central  Google Scholar 

  41. Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, Knittel K, Gieseke A, Peterknecht K, Pape T, Boetius A, Amann R, Jørgensen BB, Widdel F, Peckmann J, Pimenov NV, Gulin MB (2002) Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297:1013–1015. doi:10.1126/science.1072502

    Article  CAS  PubMed  Google Scholar 

  42. Boetius A, Elvert M, Samarkin V, Joye SB (2005) Molecular biogeochemistry of sulfate reduction, methanogenesis and the anaerobic oxidation of methane at Gulf of Mexico cold seeps. Geochim Cosmochim Ac 69:4267–4281. doi:10.1016/j.gca.2005.04.012

    Article  Google Scholar 

  43. Joye SB, Boetius A, Orcutt BN, Montoya JP, Schulz HN, Erickson MJ, Lugo SK (2004) The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps. Chem. Geol. 205:219–238. doi:10.1016/j.chemgeo.2003.12.019

    Article  CAS  Google Scholar 

  44. Marlow JJ, Steele JA, Ziebis W, Thurber AR, Levin LA, Orphan VJ (2014) Carbonate-hosted methanotrophy represents an unrecognized methane sink in the deep sea. Nat Commun 5. doi:10.1038/ncomms6094

  45. Treude T, Orphan V, Knittel K, Gieseke A, House CH, Boetius A (2007) Consumption of methane and CO2 by methanotrophic microbial mats from gas seeps of the anoxic Black Sea. Appl. Environ. Microbiol. 73:2271–2283. doi:10.1128/AEM.02685-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A (2015) Global dispersion and local diversification of the methane seep microbiome. Proc. Natl. Acad. Sci. U. S. A. 112:4015–4020. doi:10.1073/pnas.1421865112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Thornburg CC, Zabriskie TM, McPhail KL (2010) Deep-Sea hydrothermal vents: potential hot spots for natural products discovery? J. Nat. Prod. 73:489–499. doi:10.1021/np900662k

    Article  CAS  PubMed  Google Scholar 

  48. Thurber A, Sweetman A, Narayanaswamy B, Jones D, Ingels J, Hansman R (2014) Ecosystem function and services provided by the deep sea. Biogeosciences 11:3941–3963. doi:10.5194/bg-11-3941-2014

    Article  Google Scholar 

  49. Boetius A, Holler T, Knittel K, Felden J, Wenzhöfer F (2009) The seabed as natural laboratory: lessons from uncultivated methanotrophs. In: Uncultivated Microorganisms. Springer, pp 293–316. doi:10.1007/978–3–540-85465-4_15

  50. Meulepas RJ, Stams AJ, Lens PN (2010) Biotechnological aspects of sulfate reduction with methane as electron donor. Rev. Environ. Sci. Biotechnol. 9:59–78. doi:10.1007/s11157-010-9193-8

    Article  CAS  Google Scholar 

  51. Zhang Y, Arends JB, Van de Wiele T, Boon N (2011) Bioreactor technology in marine microbiology: from design to future application. Biotechnol. Adv. 29:312–321. doi:10.1016/j.biotechadv.2011.01.004

    Article  CAS  PubMed  Google Scholar 

  52. Dale AW, Aguilera D, Regnier P, Fossing H, Knab N, Jørgensen BB (2008) Seasonal dynamics of the depth and rate of anaerobic oxidation of methane in Aarhus Bay (Denmark) sediments. J. Mar. Res. 66:127–155. doi:10.1357/002224008784815775

    Article  CAS  Google Scholar 

  53. Lazar CS, Biddle JF, Meador TB, Blair N, Hinrichs KU, Teske AP (2015) Environmental controls on intragroup diversity of the uncultured benthic archaea of the miscellaneous Crenarchaeotal group lineage naturally enriched in anoxic sediments of the white Oak River estuary (North Carolina, USA). Environ. Microbiol. 17:2228–2238. doi:10.1111/1462-2920.12659

    Article  CAS  PubMed  Google Scholar 

  54. Lloyd KG, Alperin MJ, Teske A (2011) Environmental evidence for net methane production and oxidation in putative ANaerobic MEthanotrophic (ANME) archaea. Environ. Microbiol. 13:2548–2564. doi:10.1111/j.1462-2920.2011.02526.x

    Article  CAS  PubMed  Google Scholar 

  55. Hagens M, Slomp C, Meysman F, Seitaj D, Harlay J, Borges A, Middelburg J (2015) Biogeochemical processes and buffering capacity concurrently affect acidification in a seasonally hypoxic coastal marine basin. Biogeosciences 12:1561–1583. doi:10.5194/bg-12-1561-2015

    Article  CAS  Google Scholar 

  56. Egger M, Lenstra W, Jong D, Meysman FJ, Sapart CJ, van der Veen C, Röckmann T, Gonzalez S, Slomp CP (2016) Rapid sediment accumulation results in high methane effluxes from coastal sediments. PLoS One 11:e0161609. doi:10.1371/journal.pone.0161609

    Article  PubMed  PubMed Central  Google Scholar 

  57. Sulu-Gambari F, Seitaj D, Meysman FJ, Schauer R, Polerecky L, Slomp CP (2015) Cable bacteria control iron-phosphorus dynamics in sediments of a coastal Hypoxic Basin. Environ Sci Technol 50:1227–1233. doi:10.1021/acs.est.5b04369

    Article  Google Scholar 

  58. Widdel F, Bak F (1992) Gram negative mesophilic sulfate reducing bacteria. In: The Prokaryotes. Springer, New York, USA, pp 3352–3378

  59. Sipma J, Meulepas RJW, Parshina SN, Stams AJM, Lettinga G, Lens PNL (2004) Effect of carbon monoxide, hydrogen and sulfate on thermophilic (55°C) hydrogenogenic carbon monoxide conversion in two anaerobic bioreactor sludges. Appl. Microbiol. Biotechnol. 64:421–428. doi:10.1007/s00253-003-1430-4

    Article  CAS  PubMed  Google Scholar 

  60. Acree TE, Sonoff EP, Splittstoesser DF (1971) Determination of hydrogen sulfide in fermentation broths containing SO2. Appl. Environ. Microbiol. 22:110–112

    CAS  Google Scholar 

  61. APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington DC

    Google Scholar 

  62. DeLong EF (1992) Archaea in coastal marine environments. Proc. Natl. Acad. Sci. U. S. A. 89:5685–5689. doi:10.1073/pnas.89.12.5685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Song Z-Q, Wang F-P, Zhi X-Y, Chen J-Q, Zhou E-M, Liang F, Xiao X, Tang S-K, Jiang H-C, Zhang CL, Dong H, Li W-J (2013) Bacterial and archaeal diversities in Yunnan and Tibetan hot springs, China. Environ. Microbiol. 15:1160–1175. doi:10.1111/1462-2920.12025

    Article  CAS  PubMed  Google Scholar 

  64. Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402. doi:10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sneath PHA (2005) Numerical Taxonomy. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s Manual® of Systematic Bacteriology. Springer US, pp 39–42. doi:10.1007/0–387-28021-9_6

  66. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111–120. doi:10.1007/BF01731581

    Article  CAS  PubMed  Google Scholar 

  68. Schloss PD, Westcott SL (2011) Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl. Environ. Microbiol. 77:3219–3226. doi:10.1128/AEM.02810-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188–7196. doi:10.1093/nar/gkm864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Yamaguchi T, Fuchs BM, Amann R, Kawakami S, Kubota K, Hatamoto M, Yamaguchi T (2015) Rapid and sensitive identification of marine bacteria by an improved in situ DNA hybridization chain reaction (quickHCR-FISH). Syst. Appl. Microbiol. 38:400–405. doi:10.1016/j.syapm.2015.06.007

    Article  CAS  PubMed  Google Scholar 

  71. Stahl D, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons Ltd, Chichester, UK, pp 205–248

  72. Treude T, Knittel K, Blumenberg M, Seifert R, Boetius A (2005) Subsurface microbial methanotrophic mats in the Black Sea. Appl. Environ. Microbiol. 71:6375–6378. doi:10.1128/AEM.71.10.6375-6378.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Wagner M, Amann R, Lemmer H, Schleifer K-H (1993) Probing activated sludge with oligonucleotides specific for proteobacteria: inadequacy of culture-dependent methods for describing microbial community structure. Appl. Environ. Microbiol. 59:1520–1525

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Snaidr J, Amann R, Huber I, Ludwig W, Schleifer KH (1997) Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl. Environ. Microbiol. 63:2884–2896

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Vasquez-Cardenas D, van de Vossenberg J, Polerecky L, Malkin SY, Schauer R, Hidalgo-Martinez S, Confurius V, Middelburg JJ, Meysman FJ, Boschker HT (2015) Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments. ISME J 9:1966–1978. doi:10.1038/ismej.2015.10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Timmers PH, Gieteling J, Widjaja-Greefkes HA, Plugge CM, Stams AJ, Lens PN, Meulepas RJ (2015) Growth of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria in a high-pressure membrane capsule bioreactor. Appl. Environ. Microbiol. 81:1286–1296. doi:10.1128/AEM.03255-14

    Article  PubMed  PubMed Central  Google Scholar 

  77. Meulepas RJW, Jagersma CG, Zhang Y, Petrillo M, Cai H, Buisman CJ, Stams A, Lens PN (2010) Trace methane oxidation and the methane dependency of sulfate reduction in anaerobic granular sludge. FEMS Microbiol. Ecol. 72:261–271. doi:10.1111/j.1574-6941.2010.00849.x

    Article  CAS  PubMed  Google Scholar 

  78. Meulepas RJW, Jagersma CG, Khadem AF, Buisman CJN, Stams AJM, Lens PNL (2009) Effect of environmental conditions on sulfate reduction with methane as electron donor by an Eckernförde Bay enrichment. Environ Sci Technol 43:6553–6559. doi:10.1021/es900633c

    Article  CAS  PubMed  Google Scholar 

  79. Zhang Y, Henriet J-P, Bursens J, Boon N (2010) Stimulation of in vitro anaerobic oxidation of methane rate in a continuous high-pressure bioreactor. Bioresour. Technol. 101:3132–3138. doi:10.1016/j.biortech.2009.11.103

    Article  CAS  PubMed  Google Scholar 

  80. Zhang Y (2011) Microbial processes in a simulated cold seep ecosystem Ghent University, Belgium

  81. Kellermann MY, Wegener G, Elvert M, Yoshinaga MY, Lin Y-S, Holler T, Mollar XP, Knittel K, Hinrichs K-U (2012) Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities. Proc. Natl. Acad. Sci. U. S. A. 109:19321–19326. doi:10.1073/pnas.1208795109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Wegener G, Niemann H, Elvert M, Hinrichs K-U, Boetius A (2008) Assimilation of methane and inorganic carbon by microbial communities mediating the anaerobic oxidation of methane. Environ. Microbiol. 10:2287–2298. doi:10.1111/j.1462-2920.2008.01653.x

    Article  CAS  PubMed  Google Scholar 

  83. Wegener G, Krukenberg V, Ruff SE, Kellermann MY, Knittel K (2016) Metabolic capabilities of microorganisms involved in and associated with the anaerobic oxidation of methane. Front Microbiol 7. doi:10.3389/fmicb.2016.00046

  84. Aquilina A, Knab NJ, Knittel K, Kaur G, Geissler A, Kelly SP, Fossing H, Boot CS, Parkes RJ, Mills RA, Boetius A, Lloyd JR, Pancost RD (2010) Biomarker indicators for anaerobic oxidizers of methane in brackish-marine sediments with diffusive methane fluxes. Org. Geochem. 41:414–426. doi:10.1016/j.orggeochem.2009.09.009

    Article  CAS  Google Scholar 

  85. Heijs SK, Haese RR, Van der Wielen PW, Forney LJ, Van Elsas JD (2007) Use of 16S rRNA gene based clone libraries to assess microbial communities potentially involved in anaerobic methane oxidation in a Mediterranean cold seep. Microb. Ecol. 53:384–398. doi:10.1007/s00248-006-9172-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Pachiadaki MG, Lykousis V, Stefanou EG, Kormas KA (2010) Prokaryotic community structure and diversity in the sediments of an active submarine mud volcano (Kazan mud volcano, East Mediterranean Sea). FEMS Microbiol. Ecol. 72:429–444. doi:10.1111/j.1574-6941.2010.00857.x

    Article  CAS  PubMed  Google Scholar 

  87. Gonzalez-Gil G, Meulepas RJW, Lens PNL, Editor-in-Chief: Murray MY (2011) 6.33 - Biotechnological aspects of the use of methane as electron donor for sulfate reduction. In: Comprehensive Biotechnology (Second Edition). Academic Press, Burlington, pp 419–434

  88. Wang F-P, Zhang Y, Chen Y, He Y, Qi J, Hinrichs K-U, Zhang X-X, Xiao X, Boon N (2013) Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways. ISME J 8:9. doi:10.1038/ismej.2013.212

    Google Scholar 

  89. Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6:441–454. doi:10.1038/nrmicro1892

    CAS  PubMed  Google Scholar 

  90. Kleindienst S, Ramette A, Amann R, Knittel K (2012) Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments. Environ. Microbiol. 14:2689–2710. doi:10.1111/j.1462-2920.2012.02832.x

    Article  CAS  PubMed  Google Scholar 

  91. Kleindienst S, Herbst F-A, Stagars M, von Netzer F, von Bergen M, Seifert J, Peplies J, Amann R, Musat F, Lueders T (2014) Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. The ISME journal 8:2029–2044. doi:10.1038/ismej.2014.51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Vigneron A, Cruaud P, Pignet P, Caprais J-C, Gayet N, Cambon-Bonavita M-A, Godfroy A, Toffin L (2013) Bacterial communities and syntrophic associations involved in AOM process of the Sonora Margin cold seeps, Guaymas basin. Environ. Microbiol. 16:2777–2790. doi:10.1111/1462-2920.12324

    Article  PubMed  Google Scholar 

  93. 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

    Article  CAS  PubMed  Google Scholar 

  94. 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

    Article  CAS  PubMed  Google Scholar 

  95. Krüger M, Blumenberg M, Kasten S, Wieland A, Känel L, Klock J-H, Michaelis W, Seifert R (2008) A novel, multi-layered methanotrophic microbial mat system growing on the sediment of the Black Sea. Environ. Microbiol. 10:1934–1947. doi:10.1111/j.1462-2920.2008.01607.x

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge Filip Meysman from the Royal Netherlands Institute of Sea Research (NIOZ, Yerseke, The Netherlands) for providing the Lake Grevelingen sediment, Fatimah Sulu-Gambari and Mathilde Hagens (Utrecht University, The Netherlands) for the location map and Jack van de Vossenberg (UNESCO-IHE, The Netherlands) for help in FISH analysis. This research was funded by the Erasmus Mundus Joint Doctorate Program ETeCoS3 (Environmental Technologies for Contaminated Solids, Soils and Sediments, grant agreement FPA no. 2010-0009). G. Gonzalez-Gil acknowledges funding by a Marie Curie Intra European Fellowship (SUREANMetOX-300078) within the 7th European Community Framework Programme. M. Egger and C. P. Slomp acknowledge funding by the European Research Council under the European Community’s Seventh Framework Program (ERC Starting Grant #278364 to C.P. Slomp) and The Netherlands Organization for Scientific Research (NWO Vici grant 865.13.005 to C. P. Slomp). Y. Zhang acknowledges the National Natural Science Foundation of China (grant number: 41476123).

Author information

Author notes

  1. Matthias Egger

    Present address: Center for Geomicrobiology, Department of Bioscience, Aarhus University, Ny Munkegade 114, 8000, Aarhus, Denmark

Authors and Affiliations

  1. UNESCO-IHE, Westvest-7, P.O. Box 3015, Delft, 2601, DA, The Netherlands

    Susma Bhattarai, Chiara Cassarini, Graciela Gonzalez-Gil & Piet N. L. Lens

  2. Department of Earth Sciences - Geochemistry, Faculty of Geosciences, Utrecht University, P.O. Box 80021, 3508 TA, Utrecht, The Netherlands

    Matthias Egger & Caroline P. Slomp

  3. State Key Laboratory of Ocean Engineering, Shanghai Jiao Tong University, Dongchuan Rd. 800, Shanghai, 200240, People’s Republic of China

    Yu Zhang

  4. Department of Civil and Mechanical Engineering, University of Cassino and Southern Lazio, via Di Biasio 43, 03043, Cassino, FR, Italy

    Giovanni Esposito

Authors
  1. Susma Bhattarai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chiara Cassarini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Graciela Gonzalez-Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthias Egger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Caroline P. Slomp
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giovanni Esposito
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Piet N. L. Lens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susma Bhattarai.

Electronic Supplementary Material

ESM 1

(DOCX 523 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhattarai, S., Cassarini, C., Gonzalez-Gil, G. et al. Anaerobic Methane-Oxidizing Microbial Community in a Coastal Marine Sediment: Anaerobic Methanotrophy Dominated by ANME-3. Microb Ecol 74, 608–622 (2017). https://doi.org/10.1007/s00248-017-0978-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-0978-y

Keywords

search

Navigation