Time-series analysis of two hydrothermal plumes at 9°50′N East Pacific Rise reveals distinct, heterogeneous bacterial populations

Geobiology

Volumn 10, Issue 2, 2012, Pages 178-192

  Sylvan, J B ^a   Pyenson, B C ^b   Rouxel, O ^c,d   German, C R ^c   Edwards, K J ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b HAVERFORD COLLEGE   (United States)

^c WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^d UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S; SEA WATER;

BACTERIUM; COMMUNITY STRUCTURE; CORRELATION; HYDROTHERMAL PLUME; HYDROTHERMAL VENT; MICROBIAL ACTIVITY; SEAFLOOR; SEAWATER; TIME SERIES; TIMESCALE;

ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GENE LIBRARY; GENETICS; HYDROTHERMAL VENT; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; TIME;

BACTERIA; BIODIVERSITY; CLONING, MOLECULAR; DNA, BACTERIAL; ECOSYSTEM; EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GENE LIBRARY; HYDROTHERMAL VENTS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA; TIME FACTORS;

EAST PACIFIC RISE; PACIFIC OCEAN;

ALPHAPROTEOBACTERIA; AQUIFICAE; AQUIFICAE (CLASS); BACTERIA (MICROORGANISMS); EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA;

EID: 84856680618     PISSN: 14724677     EISSN: 14724669     Source Type: Journal    
DOI: 10.1111/j.1472-4669.2011.00315.x     Document Type: Article

References (68)

1. Acinas SG, Klepac-Ceraj V, Hunt DE, Pharino C, Ceraj I, Distel DL, Polz MF (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430, 551-554.
2. Adams DK, Mcgillicuddy DJ, Zamudio L, Thurnherr AM, Liang XF, Rouxel O, German CR, Mullineaux LS (2011) Surface-Generated Mesoscale Eddies Transport Deep-Sea Products from Hydrothermal Vents. Science 332, 580-583.
3. Alain K, Querellou J, Lesongeur F, Pignet P, Crassous P, Raguenes G, Cueff V, Cambon-Bonavita MA (2002) Caminibacter hydrogeniphilus gen. nov., sp nov., a novel thermophilic, hydrogen-oxidizing bacterium isolated from an East Pacific Rise hydrothermal vent. International Journal of Systematic and Evolutionary Microbiology 52, 1317-1323.
4. Antunes A, Franca L, Rainey FA, Huber R, Edwards KJ, Da Costa MS (2007) Marinobacter salsuginis sp nov., isolated from the brine-seawater interface of the Shaban Deep, Red Sea. International Journal of Systematic and Evolutionary Microbiology 57, 1035-1040.
5. Ausubel FM, Brent R, Kinsgston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1999) Short Protocols in Molecular Biology, 4th edn. Wiley, New York.
6. Bennett SA, Statham PJ, Green DRH, Le Bris N, Mcdermott J, Prado F, Rouxel OJ, Von Damm K, German CR (2011) Dissolved and particulate organic carbon in hydrothermal plumes from the East Pacific Rise, 9°50′N. Deep-Sea Research Part I-Oceanographic Research Papers 75, 5526-5539.
7. Boström K, Peterson MNA, Joensuu O, Fisher DE (1969) Aluminum-poor ferromanganoan sediments on active ocean ridges. Journal of Geophysical Research 74, 3261-3270.
8. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nature Reviews Microbiology 4, 458-468.
9. Comtet T, Jollivet D, Khripounoff A, Segonzac M (2000) Molecular and morphological identification of settlement-stage vent mussel larvae, Bathymodiolus azoricus (Bivalvia: Mytilidae), preserved in situ at active vent fields on the Mid-Atlantic Ridge. Limnology and Oceanography 45, 1655-1661.
10. Cowen JP, German CR (2003) Biogeochemical cycling in hydrothermal plumes. In Energy and Mass Transfer in Hydrothermal Systems (eds Halbach P, Tunnicliffe V, Hein J). DUP, Berlin, pp. 303-316.
11. Cowen JP, Massoth GJ, Baker ET (1986) Bacterial scavenging of Mn and Fe in a mid-field to far-field hydrothermal particle plume. Nature 322, 169-171.
12. Cowen JP, Wen XY, Jones RD, Thomson RE (1998) Elevated NH4+ in a neutrally buoyant hydrothermal plume. Deep-Sea Research Part I-Oceanographic Research Papers 45, 1891-1902.
13. Cowen JP, Bertram MA, Wakeham SG, Thomson RE, Lavelle JW, Baker ET, Feely RA (2001) Ascending and descending particle flux from hydrothermal plumes at Endeavour Segment, Juan de Fuca Ridge. Deep-Sea Research Part I-Oceanographic Research Papers 48, 1093-1120.
14. Cowen JP, Fornari DJ, Shank TM, Love B, Glazer B, Treusch AH, Holmes RC, Soule SA, Baker ET, Tolstoy M, Pomraning KR (2007) Volcanic eruptions at East Pacific Rise near 9°50′ N. Eos, Transactions, American Geophysical Union 88, 81.
15. Daffonchio D, Borin S, Brusa T, Brusetti L, Van Der Wielen P, Bolhuis H, Yakimov MM, D'auria G, Giuliano L, Marty D, Tamburini C, Mcgenity TJ, Hallsworth JE, Sass AM, Timmis KN, Tselepides A, De Lange GJ, Hubner A, Thomson J, Varnavas SP, Gasparoni F, Gerber HW, Malinverno E, Corselli C, Garcin J, Mckew B, Golyshin PN, Lampadariou N, Polymenakou P, Calore D, Cenedese S, Zanon F, Hoog S, Biodeep Sci Party (2006) Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline. Nature 440, 203-207.
16. De Angelis MA, Lilley MD, Olson EJ, Baross JA (1993) Methane oxidation in deep-sea hydrothermal plumes of the Endeavor segment of the Juan de Fuca Ridge. Deep-Sea Research Part I-Oceanographic Research Papers 40, 1169-1186.
17. DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006a) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Research 34, W394-W399.
18. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006b) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 72, 5069-5072.
19. Dick GJ, Tebo BM (2010) Microbial diversity and biogeochemistry of the Guaymas Basin deep-sea hydrothermal plume. Environmental Microbiology 12, 1334-1347.
20. Dick GJ, Clement BG, Webb SM, Fodrie FJ, Bargar JR, Tebo BM (2009) Enzymatic microbial Mn(II) oxidation and Mn biooxide production in the Guaymas Basin deep-sea hydrothermal plume. Geochimica et Cosmochimica Acta 73, 6517-6530.
21. Edwards KJ, Rogers DR, Wirsen CO, Mccollom TM (2003) Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic alpha- and, gamma-Proteobacteria from the deep sea. Applied and Environmental Microbiology 69, 2906-2913.
22. Elderfield H, Schultz A (1996) Mid-ocean ridge hydrothermal fluxes and the chemical composition of the ocean. Annual Review of Earth and Planetary Sciences 24, 191-224.
23. Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S (2006) Annually reoccurring bacterial communities are predictable from ocean conditions. Proceedings of the National Academy of Sciences of the United States of America 103, 13104-13109.
24. Gauthier MJ, Lafay B, Fernandez L, Acquaviva M, Bonin P, Bertrand J-C (1992) Marinobacter hydrocarbonoclasticus gen. nov. sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. International Journal of Systematic Bacteriology 42, 568-576.
25. German CR, Von Damm KL (2004) Hydrothermal Processes. Treatise on Geochemistry 6, 181-222.
26. German CR, Klinkhammer GP, Edmond JM, Mitra A, Elderfield H (1990) Hydrothermal scavenging of rare earth elements in the ocean. Nature 316, 516-518.
27. German CR, Colley S, Palmer MR, Khripounoff A, Klinkhammer GP (2002) Hydrothermal plume-particle fluxes at 13 degrees N on the East Pacific Rise. Deep-Sea Research Part I-Oceanographic Research Papers 49, 1921-1940.
28. German CR, Bowen A, Coleman ML, Honig DL, Huber JA, Jakuba MV, Kinsey JC, Kurz MD, Leroy S, Mcdermott JM, De Lepinay BM, Nakamura K, Seewald JS, Smith JL, Sylva SP, Van Dover CL, Whitcomb LL, Yoerger DR (2010) Diverse styles of submarine venting on the ultraslow spreading Mid-Cayman Rise. Proceedings of the National Academy of Sciences of the United States of America 107, 14020-14025.
29. Hewson I, Steele JA, Capone DG, Fuhrman JA (2006) Remarkable heterogeneity in meso- and bathypelagic bacterioplankton assemblage composition. Limnology and Oceanography 51, 1274-1283.
30. Honjo S, Dymond J, Collier R, Manganini SJ (1995) Export production of particles to the interior of the equatorial Pacific Ocean during the 1992 EqPac experiment. Deep-Sea Research Part II-Topical Studies in Oceanography 42, 831-870.
31. Huber JA, Butterfield DA, Baross JA (2003) Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiology Ecology 43, 393-409.
32. Huber JA, Johnson HP, Butterfield DA, Baross JA (2006) Microbial life in ridge flank crustal fluids. Environmental Microbiology 8, 88-99.
33. Huber JA, Mark Welch D, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318, 97-100.
34. Inagaki F, Takai K, Hideki KI, Nealson KH, Horikishi K (2003) Sulfurimonas autotrophica gen. nov., sp nov., a novel sulfur-oxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. International Journal of Systematic and Evolutionary Microbiology 53, 1801-1805.
35. Inagaki F, Takai K, Nealson KH, Horikoshi K (2004) Sulfurovum lithotrophicum gen. nov., sp nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. International Journal of Systematic and Evolutionary Microbiology 54, 1477-1482.
36. Kaye JZ, Baross JA (2000) High incidence of halotolerant bacteria in Pacific hydrothermal-vent and pelagic environments. FEMS Microbiology Ecology 32, 249-260.
37. Kaye JZ, Sylvan JB, Edwards KJ, Baross JA (2011) Halomonas and Marinobacter ecotypes from hydrothermal-vent, subseafloor and deep-sea environments. FEMS Microbiology Ecology 75, 123-133.
38. Lam P, Cowen JP, Popp BN, Jones RD (2008) Microbial ammonia oxidation and enhanced nitrogen cycling in the Endeavour hydrothermal plume. Geochimica et Cosmochimica Acta 72, 2268-2286.
39. Lane DJ (1991) 16S/23S rRNA sequencing. In Nucleic Acid Technology in Bacterial Systematics (eds Stackebrandt E, Goodfellow M). John Wiley and Sons, New York, pp. 115-175.
40. Lilley MD, Feely RA, Trefry JH (1995) Chemical and biochemical transformations in hydrothermal plumes. In Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions (eds Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE). American Geophysical Union, Washington, DC, pp. 369-391.
41. Love BA, Resing JA, Cowen JP, Lupton JE, Fornari DJ, Shank TM, Biller D (2008) Methane, manganese, and helium in hydrothermal plumes following volcanic eruptions on the East Pacific Rise near 9 degrees 50′ N. Geochemistry Geophysics Geosystems 9, Q06T01, doi:10.1029/2008GC002104.
42. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32, 1363-1371.
43. Lupton JE, Delaney JR, Johnson HP, Tivey MK (1985) Entrainment and vertical transport of deep-ocean water by buoyant hydrothermal plumes. Nature 316, 621-623.
44. Mason OU, Di Meo-Savoie CA, Van Nostrand JD, Zhou JZ, Fisk MR, Giovannoni SJ (2009) Prokaryotic diversity, distribution, and insights into their role in biogeochemical cycling in marine basalts. The ISME Journal 3, 231-242.
45. Miroshnichenko ML, L'haridon S, Schumann P, Spring S, Bonch-Osmolovskaya EA, Jeanthon C, Stackebrandt E (2004) Caminibacter profundus sp nov., a novel thermophile of Nautiliales ord. nov within the class 'Epsilonproteobacteria', isolated from a deep-sea hydrothermal vent. International Journal of Systematic and Evolutionary Microbiology 54, 41-45.
46. Mullineaux LS, Adams DK, Mills SW, Beaulieu SE (2010) Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption. Proceedings of the National Academy of Sciences of the United States of America 107, 7829-7834.
47. Nakagawa S, Takai K, Inagaki F, Chiba H, Ishibashi J, Kataoka S, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005a) Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: impacts of subseafloor phase-separation. FEMS Microbiology Ecology 54, 141-155.
48. Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005b) Distribution, phylogenetic diversity and physiological characteristics of Epsilon-Proteobacteria in a deep-sea hydrothermal field. Environmental Microbiology 7, 1619-1632.
49. Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, Howards EC, King E, Oakley CA, Reisch CR, Rinta-Kanto JM, Sharma S, Sun S, Varaljay V, Vila-Costa M, Westrich JR, Moran MA (2010) Genome characteristics of a generalist marine bacterial lineage. The ISME Journal 4, 784-798.
50. Opatkiewicz AD, Butterfield DA, Baross JA (2009) Individual hydrothermal vents at Axial Seamount harbor distinct subseafloor microbial communities. FEMS Microbiology Ecology 70, 413-424.
51. Pham VD, Konstantinidis KT, Palden T, Delong EF (2008) Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000m vertical profile in the North Pacific Subtropical Gyre. Environmental Microbiology 10, 2313-2330.
52. Rocap G, Distel DL, Waterbury JB, Chisholm SW (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Applied and Environmental Microbiology 68, 1180-1191.
53. Roth SE, Dymond J (1989) Transport and settling of organic material in a deep-sea hydrothermal plume- Evidence from particle-flux measurements. Deep-Sea Research Part I-Oceanographic Research Papers 36, 1237-1254.
54. Santelli CM, Orcutt BN, Banning E, Bach W, Moyer CL, Sogin ML, Staudigel H, Edwards KJ (2008) Abundance and diversity of microbial life in ocean crust. Nature 453, 653-657.
55. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537-7541.
56. Sievert SM, Scott KA, Klotz MG, Chain PSG, Hauser LJ, Hemp J, Hugler M, Land M, Lapidus A, Larimer FW, Lucas S, Malfatti SA, Meyer F, Paulsen IT, Ren Q, Simon J, Class USFG (2008) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Applied and Environmental Microbiology 74, 1145-1156.
57. Smith A, Popa R, Fisk M, Nielsen M, Wheat CG, Jannasch HW, Fisher AT, Becker K, Sievert SM, Flores G (2011) In situ enrichment of ocean crust microbes on igneous minerals and glasses using an osmotic flow-through device. Geochemistry Geophysics Geosystems 12, Q06007, doi:10.1029/2010GC003424.
58. Soule SA, Fornari DJ, Perfit MR, Rubin KH (2007) New insights into mid-ocean ridge volcanic processes from the 2005-2006 eruption of the East Pacific Rise, 9 degrees 46′ N-9 degrees 56′ N. Geology 35, 1079-1082.
59. Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, Chow CT, 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.
60. Sudek LA, Templeton AS, Tebo BM, Staudigel H (2009) Microbial ecology of Fe (hydr)oxide mats and basaltic rock from Vailulu'u Seamount, American Samoa. Geomicrobiology Journal 26, 581-596.
61. Sunamura M, Higashi Y, Miyako C, Ishibashi J, Maruyama A (2004) Two bacteria phylotypes are predominant in the Suiyo Seamount hydrothermal plume. Applied and Environmental Microbiology 70, 1190-1198.
62. Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T, Hirayama H, Nakagawa S, Suzuki Y, Inagaki F, Horikoshi K (2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Applied and Environmental Microbiology 71, 7310-7320.
63. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum liklihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution 28, 2731-2739.
64. Thurnherr AM, Ledwell JR, Lavelle JW, Mullineaux LS (2011) Hydrography and circulation near the crest of the East Pacific Rise between 90 degrees and 10 degrees N. Deep-Sea Research Part I-Oceanographic Research Papers 58, 365-376.
65. Tolstoy M, Cowen JP, Baker ET, Fornari DJ, Rubin KH, Shank TM, Waldhauser F, Bohnenstiehl DR, Forsyth DW, Holmes RC, Love B, Perfit MR, Weekly RT, Soule SA, Glazer B (2006) A sea-floor spreading event captured by seismometers. Science 314, 1920-1922.
66. Toner BM, Fakra SC, Manganini SJ, Santelli CM, Marcus MA, Moffet JW, Rouxel O, German CR, Edwards KJ (2009) Preservation of iron(II) by carbon-rich matrices in a hydrothermal plume. Nature Geoscience 2, 197-201.
67. Von Damm KL (2004) Evolution of the hydrothermal system at East Pacific Rise 9°50′ N: geochemical evidence for changes in the upper oceanic crust. In Mid-Ocean Ridges: Hydrothermal Interactions Between the Lithosphere and Oceans (eds German CR, Lin J, Parson LM). American Geophysical Union, Washington, DC, pp. 285-304.
68. Walsh DA, Zaikova E, Howes CG, Song YC, Wright JJ, Tringe SG, Tortell PD, Hallam SJ (2009) Metagenome of a Versatile Chemolithoautotroph from Expanding Oceanic Dead Zones. Science 326, 578-582.