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Microbial Community Composition Associated with Anaerobic Oxidation of Methane in Gas Hydrate-Bearing Sediments in the Ulleung Basin, East Sea

동해 울릉분지 가스 하이드레이트 매장 지역의 메탄산화 미생물 군집 조성 및 분포

  • Cho, Hyeyoun (Department of Marine Sciences and Convergent Technology, Hanyang University) ;
  • Kim, Sung-Han (Department of Marine Sciences and Convergent Technology, Hanyang University) ;
  • Shin, Kyung-Hoon (Department of Marine Sciences and Convergent Technology, Hanyang University) ;
  • Bahk, Jang-Jun (Petroleum and Marine Resource Research Division, Korea Institute of Geoscience and Mineral Resource) ;
  • Hyun, Jung-Ho (Department of Marine Sciences and Convergent Technology, Hanyang University)
  • 조혜연 (한양대학교 해양융합과학과) ;
  • 김성한 (한양대학교 해양융합과학과) ;
  • 신경훈 (한양대학교 해양융합과학과) ;
  • 박장준 (한국지질자원연구원 석유해저연구본부) ;
  • 현정호 (한양대학교 해양융합과학과)
  • Received : 2014.10.28
  • Accepted : 2015.02.04
  • Published : 2015.02.28

Abstract

To elucidate the microbial consortia responsible for the anaerobic methane oxidation in the methane hydrate bearing sediments, we compared the geochemical constituents of the sediment, the rate of sulfate reduction, and microbial biomass and diversity using an analysis of functional genes associated with the anaerobic methane oxidation and sulfate reduction between chimney site (UBGH2-3) on the continental slope and non-chimney site (UBGH2-10) on the basin of the Ulleung Basin. From the vertical profiles of geochemical constituents, sulfate and methane transition zone (SMTZ) was clearly defined between 0.5 and 1.5 mbsf (meters below seafloor) in the UBGH2-3, and between 6 and 7 mbsf at the UBGH2-10. At the UBGH2-3, the sulfate reduction rate (SRR) in the SMTZ exhibited was appeared to be $1.82nmol\;cm^{-3}d^{-1}$ at the depth of 1.15 mbsf. The SRR in the UBHG2-10 showed a highest value ($4.29nmol\;cm^{-3}d^{-1}$) at the SMTZ. The 16S rRNA gene copy numbers of total Prokaryotes, mcrA, (methyl coenzyme M reductase subunit A), and dsrA (dissimilatory sulfite reductase subunit A) showed the peaks in the SMTZ at both sites, but the maximum mcrA gene copy number of the UBGH2-10 appeared below the SMTZ (9.8 mbsf). ANME-1 was a predominant ANME (Anaerobic MEthanotroph) group in both SMTZs of the UBGH2-3 and -10. However, The sequences of ANME-2 were detected only at 2.2 mbsf of the UBGH2-3 where high methane flux was observed because of massive amount of gas hydrate at shallow depth. And Desulfosarcina-Desulfococcus (DSS) that is associated with ANME-2 was detected in 2.2 mbsf of the UBHG2-3. Overall results demonstrate that ANME-1 and ANME-2 are considered as significant archaeal groups related to methane cycle in the subsurface sediment of the East Sea, and ANME-2/DSS consortia might be more responsible for methane oxidation in the methane seeping region than in non-seeping region.

Acknowledgement

Grant : 가스하이드레이트 부존평가 및 저류층 특성연구, 동해 시계열 관측 및 생태환경 진단(EAST-1)

Supported by : 한국지질자원연구원, 한국해양과학기술진흥원

References

  1. Aquilina, A., N.J Knab, K. Knittel, G. Kaur, A. Geissler, S.R. Kelly, H. Fossing, C.S. Boot, R.J. Parkes, R.A. Mills, A. Boetius, J.R. Lloyd, and R.D. Pancost, 2010. Biomarker indicators for anaerobic oxidizers of methane in brackish-marine sediments with diffusive methane fluxes. Org. Geochem., 41: 414-426. https://doi.org/10.1016/j.orggeochem.2009.09.009
  2. Bertram, S., M. Blumenberg, W. Michaelis, M. Siegert, M. Kruger, and R. Seiferf, 2013. Methanogenic capabilities of ANME-archaea deduced from $^{13}C$-labelling approaches. Environ. Microbiol., 15: 2384-2393. https://doi.org/10.1111/1462-2920.12112
  3. Biddle, J.F., Z. Cardman, H. Mendlobitz, D.B. Albert, K.G. Lloyd, A. Boetius, and A. Teske, 2012. Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments. The ISME J., 6: 1018-1031. https://doi.org/10.1038/ismej.2011.164
  4. Boetius, K.A., K. Ravenschlag, C.J. Schubert, D. Rickert, F. Widdel, A. Gieseke, R. Amann, B.B. Jorgensen, U. Witte, and O. Pfannkuche, 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature, 407: 623-626. https://doi.org/10.1038/35036572
  5. Briggs, B.R., J. W. Pohlman, M. Torees, M. Riedel, E. L. Brodie, and F. S. Colwell, 2011. Macroscopic biofilms in fracture-dominated sediment that anaerobically oxidize methane. Appl. Environ. Microbiol., 77: 6780-6787. https://doi.org/10.1128/AEM.00288-11
  6. Cicerone, R.J. and R.S. Oremland, 1988. Biogeochemical aspects of atmospheric methane. Global Biochem. Cy., 2: 299-327. https://doi.org/10.1029/GB002i004p00299
  7. Dickens, G.R., 2003. Rethinking the global carbon cycle with a large, dynamic and microbially mediated gas hydrate capacitor. Earth Planet. Sci. Lett., 213: 169-183. https://doi.org/10.1016/S0012-821X(03)00325-X
  8. Deines, P., 1980. The isotope composition of reduced organic carbon. In Fritz P., Fontes J.C. (eds). Handbook of Isotope Geochemistry. The Terrestrial Environment, vol. 1.A. Elsevier, Amsterdam. pp. 329-406.
  9. Dridi. B., M.L. Fardeau, B. Olivier, D. Raoult, and M. Drancourt, 2011. The antimicrobial resistance pattern of cultured human methanogens reflects the unique phylogenetic position of archaea. J. Antimicrob. Chemother., 66: 2038-2044. https://doi.org/10.1093/jac/dkr251
  10. Fossing, H. and B.B. Jorgensen, 1989. Measurement of bacterial sulfate reduction in sediments: evaluation of a single-step chromium reduction method. Biogeochem., 8: 205-222.
  11. Gardner, J.M., A.N. Shor, and W.Y. Jung, 1998. Acoustic imagery evidence for methnae hydrates in the Ulleung Basin. Marine Geophyisical Research, 20: 495−503. https://doi.org/10.1023/A:1004716700055
  12. Harrison, B.K., H. Zhang, W. Berelson, and V.J. Orphan, 2009. Variations in archaeal and bacteria diverisity associated with the sulfatemethane transition zone in continental margin sediments (Santa Barbara Basin, California). Appl. Environ. Microbiol., 175: 1487-1499.
  13. Hoehler, T.M., M.J. Alperin, D.B. Albert, and C.S. Martens, 1994. Field and laboratory studies of methane oxidation in an anoxic marine sediment: evidence for a methanogen-sulfate reducer consortium. Global Biogeochem. Cy., 8(4): 451-463. https://doi.org/10.1029/94GB01800
  14. Hoehler, T.M., and M.J. Alperin, 1996. Anaerobic methane oxidation by a methanogen-sulfate reducer consortium: geochemical evidence and biochemical considerations. In Microbial growth on C1 compounds. Lidstrom, M.E., Tabita, F.R. (eds) Kluwer Academic Publishers, pp 326-333.
  15. Hong, W.-L., M.E. Torres, J.-H. Kim, J. Choi, and J.-J. Bahk, 2014. Towards quantifying the reaction network around the sulfatemethane- transition-zone in the Ulleung Basin, East Sea, with a kinetic modeling approach. Geochim. Cosmochim. Acta, 140: 127-141. https://doi.org/10.1016/j.gca.2014.05.032
  16. Horozal, S., G. Lee, B. Yi, D. Yoo, K. Park, H. Lee, W. Kim, H. Kim, and K. Lee, 2009. Seismic indicators of gas hydrate and associated gas in the Ulleung Basin, East Sea (Japan Sea) and implication of heat flows derived from depths of the bottom-simulating reflector. Marine Geology, 258: 126-138. https://doi.org/10.1016/j.margeo.2008.12.004
  17. Hyun, J.-H., J.-S. Mok, O.R. You, D. Kim, and D.-L. Choi, 2010. Variations and controls of sulfate reduction in the continental slope and rise of the Ulleung Basin off the southeast Korean upwelling system in the East Sea. Giomicrobiol. J., 27: 212-222. https://doi.org/10.1080/01490450903456731
  18. Inagaki, F., T. Nunoura, S. Nakagawa, A. Teske, M. Lever, A. Lauer, M. Suzuki, K. Takai, M. Delwiche, F.S. Colwell, K.H. Nealson, K. Horikoshi, S. D'Hondt, and B.B. Jorgensen, 2006. Biogeographical distribution and diversity of microbes in methane hydratebearing deep marine sediments on the Pacific Ocean Margin. Proc. Natl. Acad. Sci. USA, 103: 2815-2820. https://doi.org/10.1073/pnas.0511033103
  19. Jorgensen, B.B., 1978. A comparison of methods for quantification of bacterial sulfate reduction in coastal marine sediments. I. Measurement with radiotracer techniques. Geomicrobiol. J., 1: 11-27. https://doi.org/10.1080/01490457809377721
  20. KIGAM, 2011. Studies on Gas Hydrate Geology and Geochemistry. KIGAM Research Report (p.951). Daejeon.
  21. Knittel, K., T. Lösekann, A. Boetius, R. Kort, R. Amann, 2005. Diversity and distribution of methanotrophic archaea at cold seeps. Appl. Environ. Microbiol. 71: 467−479. https://doi.org/10.1128/AEM.71.1.467-479.2005
  22. Kvenvolden, K.A., 1988a. Methane hydrate: a major reservoir of carbon in the shallow geosphere? Chem. Geol., 71: 41-51. https://doi.org/10.1016/0009-2541(88)90104-0
  23. Kvenvolden, K.A., 1988b. Methane hydrates and global climate. Global Biogeochem. Cy., 2: 221-229. https://doi.org/10.1029/GB002i003p00221
  24. Kvenvolden, K.A., 1999. Potential effects of gas hydrate on human welfare. Proc.Natl. Acad. Sci. USA. 96: 3420-3426. https://doi.org/10.1073/pnas.96.7.3420
  25. Kondo, R., D.B. Nedwell, K.J. Purdy, and S.Q. Silva, 2004. Detection and enumeration of sulphate-reducing bacteria in estuarine sediments by competitive PCR. Geomicrobiol. J., 21: 145-157. https://doi.org/10.1080/01490450490275307
  26. Lazar, C.S., J. Dinasquet, S. L'Haridon, P. Pignet, and L. Toffin, 2011. Distribution of anaerobic methane-oxidizing and sulfate-reducing communities in the G11 Nyegga pockmark, Norwegian Sea. Antonie van Leeuwenhoek, 100: 639-653. https://doi.org/10.1007/s10482-011-9620-z
  27. Lee, J.-W., K. K. Kwon, A. Azizi, H.-M. Oh, W. Kim, J.-J. Bahk, D.- H. Lee, and J.-H. Lee, 2013a. Microbial community structures of methane hydrate-bearing sediments in the Ulleung Basin, East of Korea. Mar. Petrol. Geol., 47: 136−146. https://doi.org/10.1016/j.marpetgeo.2013.06.002
  28. Lee, D.-H., J.-H. Kim, J.-J. Bahk, H.Y. Cho, J.-H. Hyun, and K.-H. Shin, 2013b. Geochemical signature related to lipid biomarkers of ANMEs in gas hydrate-bearing sediments in the Ulleung Basin, East Sea (Korea). Mar. Petrol. Geol., 47: 125-135. https://doi.org/10.1016/j.marpetgeo.2013.06.003
  29. Leloup, J., L. Quillet, T. Berthe and F. Petit, 2006. Diversity of the dsrAB (dissimilatory sulfite reductase) gene sequences retrieved from two contrasting mudflats of the Seine estuary, France. FEMS Microbiol. Ecol., 55: 230-238. https://doi.org/10.1111/j.1574-6941.2005.00021.x
  30. Leloup, J., A. Loy, N. J. Knab, C. Borowski, M. Wagner and B. B. Jorgensen, 2007. Diversity and abundance of sulfate-reducing microorganisms in the sulfate and methane zones of a marine sediment, Black Sea. Environ. Microbiol., 9: 131-142. https://doi.org/10.1111/j.1462-2920.2006.01122.x
  31. Lim, D., J. Choi, Z. Xu, M. Kim, and D. Choi, 2009. Methane-derived authigenic carbonates from the Ulleung basin sediments, East Sea of Korea, Cont. Shelf. Res., 29: 1588-1596. https://doi.org/10.1016/j.csr.2009.04.013
  32. Lloyd, K.G., L. Lapham, and A. Teske, 2006. An anaerobic methaneoxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments. Appl. Environ. Microbiol., 72: 7218-7230. https://doi.org/10.1128/AEM.00886-06
  33. Lloyd, K.G., M.J. Alperin, and A. Teske, 2011. Environmental evidence for net methane production and oxidation in putative Anaerobic MEthanotrophioc (ANME) archaea. Environ. Microbiol., 13: 2548-2564. https://doi.org/10.1111/j.1462-2920.2011.02526.x
  34. Losekann, T., K. Knitte, T. Nadalig, B. Fuchs, H. Niemann, A. Boetius, and R. Amann, 2007. Diversity and abundance o aerobic and anaerobic methane oxidizers at the Haakon mosby mud volcano, Barents sea. Appl. Environ. Microbiol., 73: 3348-3362. https://doi.org/10.1128/AEM.00016-07
  35. Nadkarni, M.A., F.E. Martin, N.A. Kacques, and N. Hunter, 2002. Determination of bacterial load by real-time PCR using a broadrange (universal) probe and primers set. Microbiology, 148: 257-266. https://doi.org/10.1099/00221287-148-1-257
  36. Nauhaus, K., T. Treude, A. Boetius, and M. Kruger, 2005. Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ. Microbiol., 7: 98-106. https://doi.org/10.1111/j.1462-2920.2004.00669.x
  37. Niemann, H., T. Lösekann, D. Beer, M. Elvert, T. Nadalig, T. Knittel, R. Amann, E.J. Sauter, M. Schlüter, M. Klages, J.P. Foucher, and A. Boetius, 2006. Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature, 443: 854-858. https://doi.org/10.1038/nature05227
  38. Nunoura, T., H. Oida, T. Toki, J. Ashi, K. Takai, and K. Horikoshi, 2006. Quantification of mcrA by quantitative fluorescent PCR in sediments from methane seep of the Nankai Trough. FEMS Microbiol. Ecol., 57: 149-157. https://doi.org/10.1111/j.1574-6941.2006.00101.x
  39. Nunoura, T., H. Oida, J. Miyazaki, A. Miyashita, H. Imachi, and K. Takai, 2008. Quantification of mcrA by fluorescent PCR in methanogenic and anaerobic methanotrophic microbial communities. FEMS Microbiol. Ecol., 64: 240-247. https://doi.org/10.1111/j.1574-6941.2008.00451.x
  40. Orcutt, B., A. Boetius, M. Elvert, V. Samarkin, and S.B. Joye, 2005. Molecular biogeochemistry of sulfate reduction, methanogenesis and the anaerobic oxidation of methane at Gulf of Mexico cold seeps. Geochim. Comoshim. Acta 69: 4267-4281. https://doi.org/10.1016/j.gca.2005.04.012
  41. Orcutt, B., S.B. Joye, S. Kleindienst, K. Knittel, A. Ramette, A. Reitz, V. Samarkin, T. Treude, and A. Boetius, 2010. Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments. Deep-Sea Research II, 54: 2008-2021.
  42. Orphan, V.J., K.-U. Hinrichs, W. Ussler III, C.K. Paull, L.T. Taylor, S.S Sylva, J.M. Hayes, and E.F. Delong, 2001a. Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl. Environ. Microbiol., 67: 1922-1934. https://doi.org/10.1128/AEM.67.4.1922-1934.2001
  43. Orphan, V.J., C.H. House, K.U. Hinrichs, K.D. and E.F. DeLong, 2001b. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science, 293: 484-487. https://doi.org/10.1126/science.1061338
  44. Parsons, T.R., Y. Maita, and C.M. Lalli, 1984. A manual of chemical and biological methods for seawater analysis. Pergamon Press Oxford, pp 149-153.
  45. Reeburgh, W.S., 1996. "Soft spots" in the global methane budget. In Microbial growth on C1 compounds. Lidstrom, M.E., Tabita, F.R. (eds) Kluwer Academic Publishers, pp 334-342.
  46. Schippers, A. and L.N. Neretin, 2006. Quantification of microbial communities in near-surface and deeply buried marine sediments on the Peru continental margin using real-time PCR. Environ. Microbiol., 8: 1251-1260. https://doi.org/10.1111/j.1462-2920.2006.01019.x
  47. Takai, K. and K. Horikoshi, 1999. Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics. 152: 1285-1297.
  48. Teske, A., K.-U. Hinrichs, V. Edgcomb, A. de Vera Gomex, D. Kysela, S.P. Sylva, M.L. Sogin, and H.W. Jannasch, 2002. Microbial diversity of hydrothermal sediments in the Guaymas basin: Evidence for anaerobic methanotrophic communities. Appl. Environ. Microbiol., 68: 1994-2007. https://doi.org/10.1128/AEM.68.4.1994-2007.2002
  49. Treude, T., J. Niggemann, J. Kallmeyer, P. Wintersteller, C.J. Schubert, A. Boetius, and B.B. Jorgensen, 2005. Anaerobic oxidation of methane and sulfate reduction along the Chilean continental margin. Geochim. Cosmochim. Acta, 69: 2767-2779. https://doi.org/10.1016/j.gca.2005.01.002
  50. Webster, G., R.J. Parkes, J.C. Fry, and A.J. Weightman, 2004. Widespread occurrence of a novel division of bacteria identified by 16S rRNA gene sequences originally found in deep marine sediments. Appl. Environ. Microbiol., 70: 5708-5713. https://doi.org/10.1128/AEM.70.9.5708-5713.2004
  51. Webster, G., R.J. Parkes, B.A. Cragg, C.J. Newberry, and A.J. Weightman, 2006. Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru Margin. FEMS Microbiol. Ecol., 58: 65-85. https://doi.org/10.1111/j.1574-6941.2006.00147.x