First investigation of the microbiology of the deepest layer of ocean crust

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Mason, Olivia U ^a,f   Nakagawa, Tatsunori ^b,g   Rosner, Martin ^c   van Nostrand, Joy D ^d   Zhou, Jizhong ^d   Maruyama, Akihiko ^e   Fisk, Martin R ^a   Giovannoni, Stephen J ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c UNIVERSITY OF BREMEN   (Germany)

^d UNIVERSITY OF OKLAHOMA   (United States)

^e NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^f LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^g NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROCARBON; METHANE; TOLUENE; ARCHAEAL DNA; BACTERIAL DNA; RNA 16S;

ARTICLE; BIOSPHERE; CARBON FIXATION; CARBON SOURCE; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; GENE SEQUENCE; GENETIC VARIABILITY; MICROARRAY ANALYSIS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOLOGY; MOLECULAR CLONING; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OCEAN ENVIRONMENT; OXIDATION; PROTEOBACTERIA; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; ARCHAEBACTERIUM; BACTERIUM; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; GENETICS; GEOGRAPHY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; PHYLOGENY; POLYMERASE CHAIN REACTION; SEA; SEDIMENT;

PROTEOBACTERIA;

ARCHAEA; BACTERIA; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA, ARCHAEAL; DNA, BACTERIAL; ECOSYSTEM; GEOGRAPHY; GEOLOGIC SEDIMENTS; MOLECULAR SEQUENCE DATA; OCEANS AND SEAS; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; WATER MICROBIOLOGY;

EID: 78149487331     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015399     Document Type: Article

References (72)

1. Schrenk MO, Huber JA, Edwards KJ (2010) Microbial Provinces in the Subseafloor. Annu Rev Mar Sci 2: 279-304.
2. Delacour A, Früh-Green GL, Bernasconi SM, Schaeffer P, Kelley DS (2008) Carbon Geochemistry of Serpentines in the Lost City Hydrothermal System (30 °N, MAR). Geochim Cosmochim Ac 72: 3681-3702.
3. Proskurowski G, Lilley MD, Seewald JS, Früh-Green GL, Olson EJ, et al. (2008) Abiogenic Hydrocarbon Production at Lost City Hydrothermal Field. Science 319: 604-607.
4. Berndt ME, Allen DE, Seyfried WE, Jr. (1996) Reduction of CO2 during serpentinization of olivine at 300°C and 500 bar. Geology. pp 351-354.
5. Janecky DR, Seyfried WE, Jr. (1986) Hydrothermal serpentinization of peridotite within the oceanic crust: Experimental investigations of mineralogy and major element chemistry. Geochim Cosmochim Ac 50: 1357-1378.
6. Schrenk MO, Kelley DS, Bolton SA, Baross JA (2004) Low archaeal diversity linked to subseafloor geochemical processes at the Lost City Hydrothermal Field, Mid-Atlantic Ridge. Environ Microbiol 6: 1086-1095.
7. 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.
8. Fisk MR, Storrie-Lombardi MC, Douglas S, Popa R, McDonald G, et al. (2003) Evidence of biological activity in Hawaiian subsurface basalts. Geochem Geophys Geosyst 4: 10.1029/2002GC000387.
9. Lysnes K, Thorseth IH, Steinsbu BO, Øvreas L, Torsvik T, et al. (2004) Microbial community diversity in seafloor basalt from the Arctic spreading ridges. FEMS Microbiol Ecol 50: 213-230.
10. Lysnes K, Torsvik T, Thorseth IH, Pedersen RB (2004b) Microbial Populations in Ocean Floor Basalt: Results from ODP Leg 187. Proc ODP Sci Results 187: 1-27. [Online].
11. Mason OU, Di Meo-Savoie CA, Van Nostrand JD, Zhou J, Fisk MR, et al. (2009) Prokaryotic diversity, distribution, and insights into their role in biogeochemical cycling in marine basalts. ISME J 3: 231-242.
12. Mason OU, Stingl U, Wilhelm LJ, Moeseneder MM, Di Meo-Savoie CA, et al. (2007) The phylogeny of endolithic microbes associated with marine basalts. Environ Microbiol 9: 2539-2550.
13. Santelli CM, Edgcomb VP, Bach W, Edwards KJ (2009) The diversity and abundance of bacteria inhabiting seafloor lavas positively correlate with rock alteration. Environ Microbiol 11: 86-98.
14. Santelli CM, Orcutt BN, Banning E, Bach W, Moyer CL, et al. (2008) Abundance and diversity of microbial life in ocean crust. Nature 453: 653-656.
15. Thorseth IH, Torsvik T, Torsvik V, Daae FL, Pedersen RB, et al. (2001) Diversity of life in ocean floor basalt. Earth and Planet Sci Lett 194: 31-37.
16. Blackman DK, Karson JA, Kelley DS, Cann JR, Früh-Green GL, et al. (2002) Geology of the Atlantis Massif (Mid-Atlantic Ridge, 30 °N): Implications for the evolution of an ultramafic oceanic core complex. Mar Geophys Res 23: 443-469.
17. Cann JR, Blackman DK, Smith DK, McAllister E, Janssen B, et al. (1997) Corrugated slip surfaces formed at ridge-transform intersections on the Mid- Atlantic Ridge. Nature 385: 329-332.
18. He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, et al. (2007) GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J 1: 67-77.
19. Lanoil BD, Sassen R, La Duc MT, Sweet ST, Nealson KH (2001) Bacteria and Archaea Physically Associated with Gulf of Mexico Gas Hydrates. Appl Environ Microbiol 67: 5143-5153.
20. Orphan VJ, Taylor LT, Hafenbradl D, Delong EF (2000) Culture-Dependent and Culture-Independent Characterization of Microbial Assemblages Associated with High-Temperature Petroleum Reservoirs. Appl Environ Microbiol 66: 700-711.
21. Huber JA, Morrison HG, Huse SM, Neal PR, Sogin ML, et al. (2009) Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environ Microbiol 11: 1292-1302.
22. Gallego V, Garcia MT, Ventosa A (2005) Methylobacterium hispanicum sp. nov. and Methylobacterium aquaticum sp. nov., isolated from drinking water. Int J Syst Evol Microbiol 55: 281-287.
23. Van Aken B, Peres CM, Doty SL, Yoon JM, Schnoor JL (2004) Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoidesxnigra DN34). Int J Syst Evol Microbiol 54: 1191-1196.
24. Bodour AA, Wang J-M, Brusseau ML, Maier RM (2003) Temporal change in culturable phenanthrene degraders in response to long-term exposure to phenanthrene in a soil column system. Environ Microbiol 5: 888-895.
25. Perner M, Seifert R, Weber S, Koschinsky A, Schmidt K, et al. (2007) Microbial CO2 fixation and sulfur cycling associated with low-temperature emissions at the Lilliput hydrothermal field, southern Mid-Atlantic Ridge (9 degrees S). Environ Microbiol 9: 1186-1201.
26. Huber JA, Johnson HP, Butterfield DA, Baross JA (2006) Microbial life in ridge flank crustal fluids. Environ Microbiol 8: 88-99.
27. Coenye T, Goris J, De Vos P, Vandamme P, LiPuma JJ (2003) Classification of Ralstonia pickettii-like isolates from the environment and clinical samples as Ralstonia insidiosa sp. nov. Int J Syst and Evol Microbiol 53: 1075-1080.
28. Kahng H-Y, Byrne AM, Olsen RH, Kukor JJ (2000) Characterization and Role of tbuX in Utilization of Toluene by Ralstonia pickettii PKO1. J Bacteriol 182: 1232-1242.
29. Ibrahim A, GernerSmidt P, Liesack W (1997) Phylogenetic relationship of the twenty-one DNA groups of the genus Acinetobacter as revealed by 16S ribosomal DNA sequence analysis. Int J Syst Bacteriol 47: 837-841.
30. Throne-Holst M, Markussen S, Winnberg A, Ellingsen T, Kotlar H-K, et al. (2006) Utilization of n-alkanes by a newly isolated strain of Acinetobacter venetianus: the role of two AlkB-type alkane hydroxylases. Appl Microbiol and Biotechnol 72: 353-360.
31. Sentchilo VS, Perebituk AN, Zehnder AJB, van der Meer JR (2000) Molecular Diversity of Plasmids Bearing Genes That Encode Toluene and Xylene Metabolism in Pseudomonas Strains Isolated from Different Contaminated Sites in Belarus. Appl Environ Microbiol 66: 2842-2852.
32. Rojo F (2005) Specificity at the End of the Tunnel: Understanding Substrate Length Discrimination by the AlkB Alkane Hydroxylase. J Bacteriol 187: 19-22.
33. Smits THM, Rothlisberger M, Witholt B, van Beilen JB (1999) Molecular screening for alkane hydroxylase genes in Gram-negative and Gram-positive strains. Environ Microbiol 1: 307-317.
34. Einen J, Thorseth IH, Ovreas L (2008) Enumeration of Archaea and Bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy. FEMS Microbiol Lett 282: 182-187.
35. Orcutt B, Bailey B, Staudigel H, Tebo BM, Edwards KJ (2009) An interlaboratory comparison of 16S rRNA gene-based terminal restriction fragment length polymorphism and sequencing methods for assessing microbial diversity of seafloor basalts. Environ Microbiol 11: 1728-1735.
36. Mikesell MD, Kukor JJ, Olsen RH (1993) Metabolic diversity of aromatic hydrocarbon-degrading bacteria from a petroleum-contaminated aquifer. Biodegradation 4: 249-259.
37. Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, et al. (2004) Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics. Science 305: 1457-1462.
38. Park J, Kukor JJ, Abriola LM (2002) Characterization of the Adaptive Response to Trichloroethylene-Mediated Stresses in Ralstonia pickettii PKO1. Appl Environ Microbiol 68: 5231-5240.
39. Busigny V, Ader M, Cartigny P (2005) Quantification and isotopic analysis of nitrogen in rocks at the ppm level using sealed tube combustion technique: A prelude to the study of altered oceanic crust. Chem Geol 223: 249-258.
40. Dekas AE, Poretsky RS, Orphan VJ (2009) Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia. Science 326: 422-426.
41. Deutsch C, Sarmiento JL, Sigman DM, Gruber N, Dunne JP (2007) Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445: 163-167.
42. Rueter P, Rabus R, Wilkest H, Aeckersberg F, Rainey FA, et al. (1994) Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphatereducing bacteria. Nature 372: 455-458.
43. Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF, et al. (1994) Geobacter Sulfurreducens sp. nov., a hydrogen-oxidizing and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 60: 3752-3759.
44. Delacour A, Früh-Green GL, Bernasconi SM, Schaeffer P, Frank M, et al. (2008) Isotopic constraints on seawater-rock interaction and redox conditions of the gabbroic-dominated IODP Hole 1309D, Atlantis Massif (30uN, MAR). Geophys Res Abstr 10: EGU2008-A-08649.
45. Delacour A, Früh-Green GL, Frank M, Gutjahr M, Kelley DS (2008) Sr- and Nd-isotope geochemistry of the Atlantis Massif (30uN, MAR): Implications for fluid fluxes and lithospheric heterogeneity. Chem Geol 254: 19-35.
46. Kelley DS, Früh-Green GL (1999) Abiogenic methane in deep-seated mid-ocean ridge environments: Insights from stable isotope analyses. J Geophys Res 104: 10439-10460.
47. McCollom TM, Seewald JS (2006) Carbon isotope composition of organic compounds produced by abiotic synthesis under hydrothermal conditions. Earth Planet Sci Lett 243: 74-84.
48. Bird CW, Lynch JM, Pirt FJ, Reid WW, Brooks CJW, et al. (1971) Steroids and Squalene in Methylococcus capsulatus grown on Methane. Nature 230: 473-474.
49. Rohmer M, Bouvier P, O G (1979) Molecular evolution of biomembranes: structural equivalents and phylogenetic precursors of sterols. Proc Natl Acad Sci U S A 76: 847-851.
50. Neunlist S, Rohmer M (1985) Novel hopanoids from the methylotrophic bacteria Methylococcus capsulatus and Methylomonas methanica. (22S)-35-aminobacteriohopane-30,31,32,33,34-pentol and (22S)-35-amino-3 beta-methylbacteriohopane-30,31,32,33,34-pentol. Biochem J 231: 635-639.
51. Volkman JK (2003) Sterols in microorganisms. Appl Microbiol Biotechnol 60: 495-506.
52. Schouten S, Bowman JP, Rijpstra WIC, Sinninghe Damste JS (2000) Sterols in a psychrophilic methanotroph, Methylosphaera hansonii. FEMS Microbiol Lett 186: 193-195.
53. Tornabene TG, Langworthy TA, Holzer G, Oró J (1979) Squalenes, phytanes and other isoprenoids as major neutral lipids of methanogenic and thermoacidophilic "archaebacteria". J Mol Evol 13: 73-83.
54. Formisano V, Atreya S, Encrenaz T, Ignatiev N, Giuranna M (2004) Detection of Methane in the Atmosphere of Mars. Science 306: 1758-1761.
55. Atreya SK, Mahaffy PR, Wong A-S (2007) Methane and related trace species on Mars: Origin, loss, implications for life, and habitability. Planet Space Sci 55: 358-369.
56. Blackman DK, Ildefonse B, John BE, Ohara Y, Miller DJ, et al. (2006) Proc. IODP, 304/305 College Station TX: (Integrated Ocean Drilling Program Management International, Inc) doi:10.2204/iodp.proc.304305.2006.
57. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
58. Casamayor EO, Schafer H, Baneras L, Pedros-Alio C, Muyzer G (2000) Identification of and Spatio-Temporal Differences between Microbial Assemblages from Two Neighboring Sulfurous Lakes: Comparison by Microscopy and Denaturing Gradient Gel Electrophoresis. Appl Environ Microbiol 66: 499-508.
59. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At Least 1 in 20 16S rRNA Sequence Records Currently Held in Public Repositories Is Estimated To Contain Substantial Anomalies. Appl Environ Microbiol 71: 7724-7736.
60. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New Screening Software Shows that Most Recent Large 16S rRNA Gene Clone Libraries Contain Chimeras. Appl Environ Microbiol 72: 5734-5741.
61. Massana R, Murray A, Preston C, DeLong E (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63: 50-56.
62. Lane DJ (1991) 16S and 23S rRNA sequencing. In: Stackenbrandt E, Goodfellow M, eds. Nucleic acid techniques in bacterial systematics. New York: John Wiley. pp 115-148.
63. Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, et al. (1985) Rapid Determination of 16S Ribosomal RNA Sequences for Phylogenetic Analyses. Proc Natl Acad Sci 82: 6955-6959.
64. DeLong E (1992) Archaea in Coastal Marine Environments. Proc Natl Acad Sci 89: 5685-5689.
65. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2005) GenBank. Nucl Acids Res 33: D34-38.
66. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucl Acids Res 32: 1363-1371.
67. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
68. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160-174.
69. Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M, et al. (1998) Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19: 554-568.
70. Wu L, Liu X, Schadt CW, Zhou J (2006) Microarray-Based Analysis of Subnanogram Quantities of Microbial Community DNAs by Using Whole- Community Genome Amplification. Appl Environ Microbiol 72: 4931-4941.
71. Bairoch A, Apweiler R, Wu CH, Barker WC, Boeckmann B, et al. (2005) The Universal Protein Resource (UniProt). Nucl Acids Res 33: D154-159.
72. Spötl C, Vennemann TW (2003) Continuous-flow isotope ratio mass spectrometric analysis of carbonate minerals. Rapid Commun Mass Spectrom 17: 1004-1006.