Methane seep carbonates host distinct, diverse, and dynamic microbial assemblages

mBio

Volumn 6, Issue 6, 2015, Pages

  Case, David H ^a   Pasulka, Alexis L ^a   Marlow, Jeffrey J ^a   Grupe, Benjamin M ^b   Levin, Lisa A ^b   Orphan, Victoria J ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b CENTER FOR MARINE BIODIVERSITY AND CONSERVATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONIC ACID; METHANE; RNA 16S; SULFATE; WATER; CARBONIC ACID DERIVATIVE; SEA WATER;

ADVECTION; ALKALINITY; ARTICLE; BIODIVERSITY; CHLOROFLEXI; COMMUNITY ECOLOGY; CONTROLLED STUDY; GENE SEQUENCE; HABITAT; LANDSCAPE; MARINE ENVIRONMENT; METABOLISM; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; NONHUMAN; OXIDATION; PHYLOGENY; PRIORITY JOURNAL; SAMPLE; STATISTICAL ANALYSIS; WOOD; ARCHAEON; CHEMISTRY; DELTAPROTEOBACTERIA; ECOSYSTEM; GENETICS; HIGH THROUGHPUT SEQUENCING; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; SEDIMENT;

ARCHAEA; BIODIVERSITY; CARBONATES; CHLOROFLEXI; DELTAPROTEOBACTERIA; ECOSYSTEM; GEOLOGIC SEDIMENTS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; METHANE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEAWATER;

EID: 84952838094     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01348-15     Document Type: Article

References (72)

1. Niemann H, Linke P, Knittel K, MacPherson E, Boetius A, Brückmann W, Larvik G, Wallmann K, Schacht U, Omoregie E, Hilton D, Brown K, Rehder G. 2013. Methane-carbon flow into the benthic food web at cold seeps-a case study from the Costa Rica subduction zone. PLoS One 8:e74894. http://dx.doi.org/10.1371/journal.pone.0074894.
2. Thurber AR, Levin LA, Orphan VJ, Marlow JJ. 2012. Archaea in metazoan diets: implications for food webs and biogeochemical cycling. ISME J 6:1602-1612. http://dx.doi.org/10.1038/ismej.2012.16.
3. Levin L. 2005. Ecology of cold seep sediments: interactions of fauna with flow, chemistry, and microbes. Oceanogr Mar Biol Annu Rev 43:1-46. http://dx.doi.org/10.1201/9781420037449.ch1.
4. Hinrichs KU, Hayes JM, Sylva SP, Brewer PG, DeLong EF. 1999. Methane-consuming archaebacteria in marine sediments. Nature 398: 802-805. http://dx.doi.org/10.1038/19751.
5. Orphan VJ, Hinrichs K, 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. http://dx.doi.org/10.1128/ AEM.67.4.1922-1934.2001.
6. Pop Ristova P, Wenzhöfer F, Ramette A, Felden J, Boetius A. 2015. Spatial scales of bacterial community diversity at cold seeps (Eastern Mediterranean Sea). ISME J 9:1306-1318. http://dx.doi.org/10.1038/ ismej.2014.217.
7. Nunoura T, Takaki Y, Kazama H, Hirai M, Ashi J, Imachi H, Takai K. 2012. Microbial diversity in deep-sea methane seep sediments presented by SSU rRNA gene tag sequencing. Microbes Environ 27:382-390. http:// dx.doi.org/10.1264/jsme2.ME12032.
8. Ruff SE, Arnds J, Knittel K, Amann R, Wegener G, Ramette A, Boetius A. 2013. Microbial communities of deep-sea methane seeps at Hikurangi Continental margin (New Zealand). PLoS One 8:e72627. http:// dx.doi.org/10.1371/journal.pone.0072627.
9. Marlow JJ, Steele JA, Case DH, Connon SA, Levin LA, Orphan VJ. 2014. Microbial abundance and diversity patterns associated with sediments and carbonates from the methane seep environments of Hydrate Ridge, OR. Front Mar Sci 1:1-16. http://dx.doi.org/10.3389/fmars.2014.00044.
10. 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. http://dx.doi.org/ 10.1073/pnas.1421865112.
11. Stadnitskaia A, Muyzer G, Abbas B, Coolen MJL, Hopmans EC, Baas M, van Weering TCE, Ivanov MK, Poludetkina E, Sinninghe Damsté JS. 2005. Biomarker and 16S rDNA evidence for anaerobic oxidation of methane and related carbonate precipitation in deep-sea mud volcanoes of the Sorokin Trough, Black Sea. Mar Geol 217:67-96. http://dx.doi.org/ 10.1016/j.margeo.2005.02.023.
12. Thiel V, Peckmann J, Richnow HH, Luth U, Reitner J, Michaelis W. 2001. Molecular signals for anaerobic methane oxidation in Black Sea seep carbonates and a microbial mat. Mar Chem 73:97-112. http://dx.doi.org/ 10.1016/S0304-4203(00)00099-2.
13. Heijs SK, Aloisi G, Bouloubassi I, Pancost RD, Pierre C, Sinninghe Damsté JS, Gottschal JC, van Elsas JD, Forney LJ. 2006. Microbial community structure in three deep-sea carbonate crusts. Microb Ecol 52: 451-462. http://dx.doi.org/10.1007/s00248-006-9099-8.
14. Gieskes J, Mahn C, Day S, Martin JB, Greinert J, Rathburn T, McAdoo B. 2005. A study of the chemistry of pore fluids and authigenic carbonates in methane seep environments: Kodiak Trench, Hydrate Ridge, Monterey Bay, and Eel River Basin. Chem Geol 220:329-345. http://dx.doi.org/ 10.1016/j.chemgeo.2005.04.002.
15. Greinert J, Bohrmann G, Suess E. 2001. Gas hydrate-associated carbonates and methane-venting at Hydrate Ridge: classification, distribution, and origin of authigenic lithologies, p 99-113. In Paull CK, Dillon WP (ed), Natural gas hydrates. American Geophysical Union, Washington, DC.
16. 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 J Commun 5:5094.
17. Marlow J, Peckmann J, Orphan V. 2015. Autoendoliths: a distinct type of rock-hosted microbial life. Geobiology 13:303-307. http://dx.doi.org/ 10.1111/gbi.12131.
18. Levin LA, Mendoza GF, Grupe BM, Gonzalez JP, Jellison B, Rouse G, Thurber AR, Waren A. 2015. Biodiversity on the rocks: macrofauna inhabiting authigenic carbonate at Costa Rica methane seeps. PLoS One 10:1-31. http://dx.doi.org/10.1371/journal.pone.0131080.
19. Mason OU, Case DH, Naehr TH, Lee RW, Thomas RB, Bailey JV, Orphan VJ. 2015. Comparison of archaeal and bacterial diversity in methane seep carbonate nodules and host sediments, Eel River Basin and Hydrate Ridge, USA. Microb Ecol 70:766-784. http://dx.doi.org/10.1007/ s00248-015-0615-6.
20. Chen Z, Yan W, Chen M, Wang S, Lu J, Zhang F, Xiang R, Xiao S, Yan P, Gu S. 2006. Discovery of seep carbonate nodules as new evidence for gas venting on the northern continental slope of South China sea. Chin Sci Bull 51:1228-1237. http://dx.doi.org/10.1007/s11434-006-1228-8.
21. Watanabe Y, Nakai S, Hiruta A, Matsumoto R, Yoshida K. 2008. U-Th dating of carbonate nodules from methane seeps off Joetsu, Eastern margin of Japan Sea. Earth Planet Sci Lett 272:89-96. http://dx.doi.org/ 10.1016/j.epsl.2008.04.012.
22. Hovland M, Talbot MR, Qvale H, Olaussen S, Aasberg L. 1987. Methane-related carbonate cements in pockmarks of the North Sea. J Sedimentary Petrology 57:881-892.
23. Naehr TH, Eichhubl P, Orphan VJ, Hovland M, Paull CK, Ussler W, Lorenson TD, Greene HG. 2007. Authigenic carbonate formation at hydrocarbon seeps in continental margin sediments: a comparative study. Deep Sea Res II 54:1268-1291. http://dx.doi.org/10.1016/ j.dsr2.2007.04.010.
24. Teichert BMA, Bohrmann G, Suess E. 2005. Chemoherms on Hydrate Ridge-unique microbially-mediated carbonate build-ups growing into the water column. Palaeogeogr Palaeoclimatol Palaeoecol 227:67-85. http://dx.doi.org/10.1016/j.palaeo.2005.04.029.
25. Sahling H, Masson DG, Ranero CR, Hühnerbach V, Weinrebe W, Klaucke I, Bürk D, Brückmann W, Suess E. 2008. Fluid seepage at the continental margin offshore Costa Rica and southern Nicaragua. Geochem Geophys Geosyst 9:Q05S05. http://dx.doi.org/10.1029/ 2008GC001978.
26. Birgel D, Himmler T, Freiwald A, Peckmann J. 2008. A new constraint on the antiquity of anaerobic oxidation of methane: late Pennsylvanian seep limestones from southern Namibia. Geology 36:543-546. http:// dx.doi.org/10.1130/G24690A.1.
27. Tryon MD, Brown KM, Torres ME. 2002. Fluid and chemical flux in and out of sediments hosting methane hydrate deposits on Hydrate Ridge, OR, II: hydrological processes. Earth Planet Sci Lett 201:541-557. http:// dx.doi.org/10.1016/S0012-821X(02)00732-X.
28. Tryon MD, Brown KM, Torres ME, Tréhu AM, McManus J, Collier RW. 1999. Measurements of transience and downward fluid flow near episodic methane gas vents, Hydrate Ridge, Cascadia. Geology 27:1075-1078. http:// dx.doi.org/10.1130/0091-7613(1999)027_1075:MOTADF_2.3.CO;2.
29. Bekins BA, Dreiss SJ. 1992. A simplified analysis of parameters controlling dewatering in accretionary prisms. Earth Planet Science Lett 109: 275-287. http://dx.doi.org/10.1016/0012-821X(92)90092-A.
30. Orphan VJ, Ussler W, Naehr TH, House CH, Hinrichs K, 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. http://dx.doi. org/1 0. 1 0 1 6 / j.chemgeo.2003.12.035.
31. Boetius A, Suess E. 2004. Hydrate Ridge: a natural laboratory for the study of microbial life fueled by methane from near-surface gas hydrates. Chem Geol 205:291-310. http://dx.doi.org/10.1016/j.chemgeo.2003.12.034.
32. Rossel PE, Elvert M, Ramette A, Boetius A, Hinrichs K. 2011. Factors controlling the distribution of anaerobic methanotrophic communities in marine environments: evidence from intact polar membrane lipids. Geochim Cosmochim Acta 75:164-184. http://dx.doi.org/10.1016/ j.gca.2010.09.031.
33. Bowman JP, McCuaig RD. 2003. Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl Environ Microbiol 69:2463-2483. http://dx.doi.org/ 10.1128/AEM.69.5.2463-2483.2003.
34. Schauer R, Bienhold C, Ramette A, Harder J. 2010. Bacterial diversity and biogeography in deep-sea surface sediments of the south Atlantic Ocean. ISME J 4:159-170. http://dx.doi.org/10.1038/ismej.2009.106.
35. Li L, Kato C, Horikoshi K. 1999. Microbial diversity in sediments collected from the deepest cold-seep area, the Japan Trench. Mar Biotechnol 1:391-400. http://dx.doi.org/10.1007/PL00011793.
36. Ijiri A, Tsunogai U, Gamo T, Nakagawa F, Sakamoto T, Saito S. 2009. Enrichment of adsorbed methane in authigenic carbonate concretions of the Japan Trench. Geo-Marine Lett 29:301-308. http://dx.doi.org/ 10.1007/s00367-009-0143-9.
37. Blumenberg M, Walliser E, Taviani M, Seifert R, Reitner J. 2015. Authigenic carbonate formation and its impact on the biomarker inventory at hydrocarbon seeps-a case study from the Holocene Black sea and the plio-Pleistocene Northern Apennines (Italy). Mar Petrol Geol 66: 532-541. http://dx.doi.org/10.1016/j.marpetgeo.2015.05.013.
38. Treude T, Boetius A, Knittel K, Wallmann K, Jørgensen B. 2003. Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific Ocean. Mar Ecol Prog Ser 264:1-14. http://dx.doi.org/10.3354/ meps264001.
39. Sylvan JB, Toner BM, Edwards KJ. 2012. Life and death of deep-sea vents: bacterial diversity and ecosystem succession on inactive hydrothermal sulfides. mBio 3:e00279-11. http://dx.doi.org/10.1128/mBio.00279-11.
40. Alain K, Zbinden M, Le Bris N, Lesongeur F, Quérellou J, Gaill F, Cambon-Bonavita. 2004. Early steps in microbial colonization processes at deep-sea hydrothermal vents. Environ Microbiol 6:227-241. http:// dx.doi.org/10.1111/j.1462-2920.2003.00557.x.
41. Sylvan JB, Pyenson BC, Rouxel O, German CR, Edwards KJ. 2012. Time-series analysis of two hydrothermal plumes at 9°50=N East Pacific Rise reveals distinct, heterogeneous bacterial populations. Geobiology 10: 178-192. http://dx.doi.org/10.1111/j.1472-4669.2011.00315.x.
42. Garrity GM, et al. (ed). 2005. The Proteobacteria. Bergey's manual of systematic bacteriology, vol 2. Springer Verlag, New York, NY.
43. Sorokin DY, Tourova TP, Bezsoudnova EY, Pol A, Muyzer G. 2007. Denitrification in a binary culture and thiocyanate metabolism in Thiohalophilus thiocyanoxidans gen. nov. sp. nov.-a moderately halophilic chemolithoautotrophic sulfur-oxidizing Gammaproteobacterium from hypersaline lakes. Arch Microbiol 187:441-450. http://dx.doi.org/ 10.1007/s00203-006-0208-3.
44. Morono Y, Terada T, Nishizawa M, Ito M, Hillion F, Takahata N, Sano Y, Inagaki F. 2011. Carbon and nitrogen assimilation in deep subseafloor microbial cells. Proc Natl Acad Sci U S A 108:18295-18300. http:// dx.doi.org/10.1073/pnas.1107763108.
45. Orphan VJ, Turk KA, Green AM, House CH. 2009. Patterns of 15N assimilation and growth of methanotrophic ANME-2 archaea and sulfatereducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environ Microbiol 11:1777-1791. http://dx.doi.org/10.1111/ j.1462-2920.2009.01903.x.
46. Girguis PR, Orphan VJ, Hallam SJ, DeLong EF. 2003. Growth and methane oxidation rates of anaerobic methanotrophic archaea in a continuous-flow bioreactor. Appl Environ Microbiol 69:5472-5482. http://dx.doi.org/10.1128/AEM.69.9.5472-5482.2003.
47. Rajala P, Bomberg M, Kietäväinen R, Kukkonen I, Ahonen L, Nyyssönen M, Itävaara M. 2015. Rapid reactivation of deep subsurface microbes in the presence of C-1 compounds. Microorganisms 3:17-33. http://dx.doi.org/10.3390/microorganisms3010017.
48. Bernard C, Fenchel T. 1995. Mats of colourless sulphur bacteria. II. Structure, composition of biota and successional patterns. Mar Ecol Prog Ser 128:171-179. http://dx.doi.org/10.3354/meps128171.
49. Sievert SM, Wieringa EBA, Wirsen CO, Taylor CD. 2007. Growth and mechanism of filamentous-sulfur formation by Candidatus Arcobacter sulfidicus in opposing oxygen-sulfide gradients. Environ Microbiol 9:271-276. http://dx.doi.org/10.1111/j.1462-2920.2006.01156.x.
50. Schmale O, Leifer I, Schneider von Deimling J, Stolle C, Krause S, Kießlich K, Frahm A, Treude T. 2015. Bubble transport mechanism: indications for a gas bubble-mediated inoculation of benthic methanotrophs into the water column. Contin Shelf Res 103:70-78. http:// dx.doi.org/10.1016/j.csr.2015.04.022.
51. Taylor CD, Wirsen CO, Gaill F. 1999. Rapid microbial production of filamentous sulfur mats at hydrothermal vents. Appl Environ Microbiol 65:2253-2255.
52. 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. http://dx.doi.org/10.1128/AEM.71.1.467-479.2005.
53. Reitner J, Peckmann J, Reimer A, Schumann G, Thiel V. 2005. Methanederived carbonate build-ups and associated microbial communities at cold seeps on the lower Crimean shelf (Black Sea). Facies 51:66-79. http:// dx.doi.org/10.1007/s10347-005-0059-4.
54. Bienhold C, Pop Ristova P, Wenzhöfer F, Dittmar T, Boetius A. 2013. How deep-sea wood falls sustain chemosynthetic life. PLoS One 8:e53590. http://dx.doi.org/10.1371/journal.pone.0053590.
55. Distel DL, Baco AR, Chuang E, Morrill W, Cavanaugh C, Smith CR. 2000. Marine ecology: do mussels take wooden steps to deep-sea vents? Nature 403:725-726. http://dx.doi.org/10.1038/35001667.
56. Fagervold SK, Romano C, Kalenitchenko D, Borowski C, Nunes-Jorge A, Martin D, Galand PE. 2014. Microbial communities in sunken wood are structured by wood-boring bivalves and location in a submarine canyon. PLoS One 9:e96248. http://dx.doi.org/10.1371/ journal.pone.0096248.
57. Fagervold SK, Galand PE, Zbinden M, Gaill F, Lebaron P, Palacios C. 2012. Sunken woods on the ocean floor provide diverse specialized habitats for microorganisms. FEMS Microbiol Ecol 82:616-628. http:// dx.doi.org/10.1111/j.1574-6941.2012.01432.x.
58. Suess E, Carson B, Ritger SD, Moore JC, Jones ML, Kulm LD, Cochrane GR. 1985. Biological communities at vent sites along the subduction zone off Oregon. Bull Biol Soc Wash 6:475-484.
59. 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. http://dx.doi.org/10.1038/35036572.
60. Sahling H, Rickert D, Lee R, Linke P, Suess E. 2002. Macrofaunal community structure and sulfide flux at gas hydrate deposits from the Cascadia convergent margin, NE Pacific. Mar Ecol Prog Ser 231:121-138. http://dx.doi.org/10.3354/meps231121.
61. Levin LA, Mendoza GF, Gonzalez JP, Thurber AR, Cordes EE. 2010. Diversity of bathyal macrofauna on the northeastern Pacific margin: the influence of methane seeps and oxygen minimum zones. Mar Ecol 31: 94-110. http://dx.doi.org/10.1111/j.1439-0485.2009.00335.x.
62. Guilini K, Levin LA, Vanreusel A. 2012. Cold seep and oxygen minimum zone associated sources of margin heterogeneity affect benthic assemblages, diversity and nutrition at the Cascadian margin (NE Pacific Ocean). Prog Oceanogr 96:77-92. http://dx.doi.org/10.1016/ j.pocean.2011.10.003.
63. Levin LA, Orphan VJ, Rouse GW, Rathburn AE, Ussler W, Cook GS, Goffredi SK, Perez EM, Waren A, Grupe BM, Chadwick G, Strickrott B. 2012. A hydrothermal seep on the Costa Rica margin: middle ground in a continuum of reducing ecosystems. Proc R Soc Lond 279:2580-2588. http://dx.doi.org/10.1098/rspb.2012.0205.
64. Dekas AE, Chadwick GL, Bowles MW, Joye SB, Orphan VJ. 2014. Spatial distribution of nitrogen fixation in methane seep sediment and the role of the ANME archaea. Environ Microbiol 16:3012-3029. http:// dx.doi.org/10.1111/1462-2920.12247.
65. Levin L, Ziebis W, Mendoza G, Growney V, Tryon M, Brown K, Mahn C, Gieskes J, Rathburn A. 2003. Spatial heterogeneity of macrofauna at northern California methane seeps: influence of sulfide concentration and fluid flow. Mar Ecol 265:123-139. http://dx.doi.org/10.3354/ meps265123.
66. 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. http://dx.doi.org/10.1038/ ismej.2009.155.
67. Gilbert JA, Meyer F, Jansson J, Gordon J, Pace NR, Tiedje JM, Ley RE, Fierer N, Field D, Kyrpides NC, Gloeckner FO, Klenk HP, Wommack KE, Glass E, Docherty K, Gallery R, Stevens R, Knight R. 2011. The Earth Microbiome Project: meeting report of the "1st EMP meeting on sample selection and acquisition" at Argonne National Laboratory, October 6th, 2010, p 1-5.
68. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Nalt Acad Sci U S A 108:4516-4522. http://dx.doi.org/10.1073/pnas.1000080107.
69. 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. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621-1624. http://dx.doi.org/10.1038/ismej.2012.8.
70. R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
71. Clarke KR, Warwick RM. 2001. Change in marine communities, 2nd ed. Primer-E Ltd., Plymouth, United Kingdom.
72. Ryan WBF, Carbotte SM, Coplan JO, O'Hara S, Melkonian A, Arko R, Weissel RA, Ferrini V, Goodwillie A, Nitsche F, Bonczkowski J, Zemsky R. 2009. Global multi-resolution topography synthesis. Geochem Geophys Geosyst 10:1-9.