Microbial utilization of abiogenic carbon and hydrogen in a serpentinite-hosted system

Geochimica et Cosmochimica Acta

Volumn 92, Issue , 2012, Pages 82-99

  Lang, Susan Q ^a   Früh Green, Gretchen L ^a   Bernasconi, Stefano M ^a   Lilley, Marvin D ^b   Proskurowski, Giora ^b   Méhay, Sabine ^a   Butterfield, David A ^b,c  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOTROPHY; CARBON; CONCENTRATION (COMPOSITION); HOST ROCK; HYDROGEN; HYDROTHERMAL ACTIVITY; HYDROTHERMAL DEPOSIT; HYDROTHERMAL SYSTEM; HYPOTHESIS TESTING; METHANE; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; REACTION KINETICS; REDUCTION; SERPENTINITE; SULFATE;

ATLANTIC OCEAN; LOST CITY HYDROTHERMAL FIELD;

METHANOSARCINALES;

EID: 84864072965     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2012.06.006     Document Type: Article

References (87)

1. Abrajano T.A., Sturchio N.C., Bohlke J.K., Lyon G.L., Poreda R.J., Stevens C.M. Methane-hydrogen gas seeps, Zambales Ophiolite, Philippines: deep or shallow origin?. Chem. Geol. 1988, 71:211-222.
2. Alperin M.J., Hoehler T.M. Anaerobic methane oxidation by archaea/sulfate reducing bacteria aggregates: 1. Thermodynamic and physical constraints. Am. J. Sci. 2009, 309:869-957.
3. Alperin M.J., Hoehler T.M. Anaerobic methane oxidation by archaea/sulfate reducing bacteria aggregates: 2. Isotopic constraints. Am. J. Sci. 2009, 309:958-984.
4. 2 during serpentinization of olivine at 300 degrees C and 500bar. Geology 1996, 24:351-354.
5. Boschi C., Dini A., Früh-Green G.L., Kelley D.S. Isotopic and element exchange during serpentinization and metasomatism at the Atlantis Massif (MAR 30 degrees N): insights from B and Sr isotope data. Geochem. Cosmochim. Acta 2008, 72:1801-1823.
6. Bradley A.S., Hayes J.M., Summons R.E. Extraordinary C-13 enrichment of diether lipids at the Lost City Hydrothermal Field indicates a carbon-limited ecosystem. Geochim. Cosmochim. Acta 2009, 73:102-118. 10.1016/j.gca.2008.10.005.
7. Brazelton W.J., Schrenk M.O., Kelley D.S., Baross J.A. Methane- and sulfur-metabolizing microbial communities dominate the Lost City Hydrothermal Field ecosystem. Appl. Environ. Microbiol. 2006, 72:6257-6270.
8. Brazelton W.J., Mehta M.P., Kelley D.S., Baross J.A. Physiological differentiation within a single-species biofilm fueled by serpentinization. Biology 2011, 2(4). 10.1128/mbio.00127-11.
9. Butterfield, et al. Mixing, reaction and microbial activity in the sub-seafloor revealed by temporal and spatial variation in diffuse flow vents at axial volcano. The Subseafloor Biosphere at Mid-ocean Ridges; Geophys. 98 Monogr. 2004, vol. 144. AGU.
10. Campbell L.L., Postgate J.R. Classification of the spore-forming sulfate-reducing bacteria. Bacteriol. Rev. 1965, 29:359-363.
11. Cannat M. Emplacement of mantle rocks in the seafloor at mid-ocean ridges. J. Geophys. Res. 1993, 98:4163-4172.
12. Cannat M., Fontaine F., Escartin J. Serpentinization and associated hydrogen and methane fluxes at slow-spreading ridges. Diversity of Hydrothermal Systems on Slow Spreading Ocean Ridges; Geophys. Monogr. 2010, vol. 188. AGU.
13. Charlou J.L., Donval J.P. Hydrothermal methane venting between 12-degrees-N and 26-degrees-N along the mid-Atlantic Ridge. J. Geophys. Res. - Solid Earth 1993, 98:9625-9642.
14. 4 plumes generated by serpentinization of ultramafic rocks at the intersection of the 15 degrees 20'N fracture zones and the Mid-Atlantic Ridge. Geochim. Cosmochim. Acta 1998, 62:2323-2333.
15. 4 vent fluids issuing from ultra-mafic rocks at the Rainbow hydrothermal field (36°14'N, MAR). Chem. Geol. 2002, 191:345-359.
16. 4 and evidence of abiotic hydrocarbon synthesis by serpentinization in ultramafic-hosted hydrothermal systems on the Mid-Atlantic Ridge. Diversity of Hydrothermal Systems on Slow Spreading Ocean Ridges; Geophys. Monogr. Ser., 188 2010, AGU. P. Rona, C.W. Devey, J. Dyment, B.J. Murton (Eds.).
17. Cline J.D. Spectrophotometeric determiniation of hydrogen sulfide in natural waters. Limnol. Oceanogr. 1969, 14:454-458.
18. DeChaine E.G., Bates A.E., Shank T.M., Cavanaugh C.M. Off-axis symbiosis found: characterization and biogeography and bacterial symbionts of Bathymodiols mussels from Lost City hydrothermal vents. Environ. Microbiol. 2006, 8:1902-1912.
19. Delacour A., Früh-Green G.L., Bernasconi S.M., Kelley D.S. Sulfur in peridotites and gabbros at Lost City (30°N, MAR): implications for hydrothermal alteration and microbial activity during serpentinization. Geochim. Cosmochim. Acta 2008, 72:5090-5110.
20. Dick H.B.J. Abyssal peridotites, very slow spreading reidges and ocean ridge magmatism, in Magmatism in the Ocean Basins (eds. S.D. Saunders and M.J. Norry). Geol. Soc. Lond. Spec. Publ. 1989, 42:71-105.
21. Dick H.B.J., Lin J., Schouten H. An ultraslow-spreading class of ocean ridge. Nature 2003, 426:405-412.
22. Dick H.B.J., Tivey M.A., Tucholke B.E. Plutonic foundation of a slow-spreading ridge segment: Oceanic core complex at Kane Megamullion, 23 degrees 30N, 45 degrees 20W. Geochem. Geophys. Geosyst. 2008, 9:Q05014.
23. Druffel E.R.M., Williams P.M., Bauer J.E., Ertel J.R. Cycling of dissolved and particulate organic-matter in the open ocean. J. Geophys. Res. Oceans 1992, 97:15639-15659.
24. Druffel E.R.M., Bauer J.E., Griffin S., Beaupre S.R., Hwang J. Dissolved inorganic radiocarbon in the North Pacific Ocean and Sargasso Sea. Deep-Sea Res. Part I - Oceanographic Res. Papers 2008, 55:451-459.
25. 25 irregular isoprenoids. Naturwissenschaften 1999, 86:295-300.
26. Emmanuel S., Ague J.J. Implications of present-day abiogenic methane fluxes for the early Archean atmosphere. Geophys. Res. Lett. 2007, 34:L15810.
27. Foustoukos D.I., Seyfried W.E. Hydrocarbons in hydrothermal vent fluids: the role of chromium-bearing catalysts. Science 2004, 304:1002-1005.
28. Fritz P., Clark I.D., Fontes J.C., Whiticar M.J., Faber E. Deuterium and 13C evidence for low temperature production of hydrogen and methane in a highly alkaline groundwater environment in Oman. Water-Rock Interaction 1992, Balkama, Rotterdam. Kharaka, Maest (Eds.).
29. Früh-Green G.L., Kelley D.S., Bernasconi S.M., Karson J.A., Ludwig K.A., Butterfield D.A., Boschi C., Proskurowski G. 30,000years of hydrothermal activity at the Lost City vent field. Science 2003, 310:495-498.
30. Früh-Green G.L., Connolly J.A.D., Plas A., Kelley D.S., Grobéty B. Serpentinization of oceanic peridotites: implications for geochemical cycles and biological activity. The Subseafloor Biosphere at Mid-ocean Ridges; Geophys. 98 Monogr. 2004, Vol. 144. AGU.
31. Gerasimchuk A.L., et al. The search for sulfate-reducing bacteria in mat samples from the Lost City Hydrothermal Field by molecular cloning. Microbiology 2010, 79:96-105.
32. German C.R., Bowen A., Coleman M.L., Honig D.L., Huber J.A., Jakuba M.V., Kinsey J.C., Kurz M.D., Leroy S., McDermott J.M., de Lepinay B.M., Nakamura K., Seewald J.S., Smith J.L., Sylva S.P., Van Dover C.L., Whitcomb L.L., Yoerger D.R. Diverse styles of submarine venting on the ultraslow spreading Mid-Cayman Rise. Proc. Natl. Acad. Sci. USA 2010, 107:14020-14025.
33. Hedderich R., Whitman W.B. Physiology and biochemistry of the methane-producing archaea. The Prokaryotes 2006, vol. 2. Springer, New York.
34. Hinrichs K.-U., Hayes J.M., Sylva S.P., Brewer P.G., DeLong E.F. Methane-consuming archaebacteria in marine sediments. Nature 1999, 398:802-805.
35. Hoehler T.M., Alperin M.J., Albert D.B., Martens C.S. Field and laboratory studies of methane oxidation in an anoxic marine sediment: evidence for a methanogen-sulfate reducer consortium. Global Biogeochem. Cycles 1994, 8:451-463.
36. Holm N.G., Andersson E.M. Organic molecules on the early Earth: hydrothermal systems. The Molecular Origins of Life 1998, 86-99. Cambridge University Press. A. Brack (Ed.).
37. Holm N.G., Charlou J.L. Initial indications of abiotic formation of hydrocarbons in the Rainbow ultramafic hydrothermal system, Mid-Atlantic Ridge. Earth Planet. Sci. Lett. 2001, 191:1-8.
38. House C.H., Schopf J.W., Stetter K.O. Carbon isotopic fractionation by Archaeans and other thermophilic prokaryotes. Org. Geochem. 2003, 34:345-356.
39. Jahnke L.L., Summons R.E., Hope J.M., des Marais D.J. Carbon isotopic fractionation in lipids from methanotrophic bacteria II: the effects of physiology and environmental parameters on the biosynthesis and isotopic signatures of biomarkers. Geochim. Cosmochim. Acta 1999, 63:79-93.
40. Junier P., et al. The genome of the Gram-positive metal- and sulfate-reducing bacterium Desulfotomaculum reducens strain MI-1. Environ. Microbiol. 2010, 12:2738-2754.
41. Jansen K., Thauer R.K., Widdel F., Fuchs G. Carbon assimilation pathways in sulfate reducing bacteria - formate, carbon-dioxide, carbon-monoxide, and acetate assimilation by Desulfovibrio baarsii. Arch. Microbiol. 1984, 138:257-262.
42. Johnson J.W., Oelkers E.H., Helgeson H.C. SUPCRT92: a software package for calculating the standard molal thermodynamic properties of minerals, gases, aqueous species, and reactions from 1 to 5000bar and 0 to 1000°C. Comput. Geosci. 1992, 18:899-947.
43. Junier P., Junier T., Podell S., Sims D.R., Detter J.C., Lykidis A., Han C.S., Wigginton N.S., Gaasterland T., Bernier-Latmani R. The genome of the Gram-positive metal- and sulfate-reducing bacterium Desulfotomaculum reducens strain MI-1. Environ. Microbiol. 2010, 12:2738-2754.
44. Karpov I.K., Chudnenko K.V., Kulik D.A. Modeling chemical mass-transfer in geochemical processes: thermodynamic relations, conditions of equilibria and numerical algorithms. Am. J. Sci. 1997, 297:767-806.
45. Kasting J.F., Catling D. Evolution of a habitable planet. Annu. Rev. Astron. Astrophys. 2003, 41:429-463.
46. Keir R.S. A note on the fluxes of abiogenic methane and hydrogen from mid-ocean ridges. Geophys. Res. Lett. 2010, 37:L24609.
47. Kelley D.S., et al. An off-axis hydrothermal vent field near the Mid-Atlantic ridge at 30 degrees N. Nature 2001, 412:145-149.
48. Kelley D.S., et al. A serpentinite-hosted ecosystem: the Lost City Hydrothermal Field. Science 2005, 307:1428-1434.
49. Kennedy P., Kennedy H., Papadimitriou S. The effect of acidification on the determination of organic carbon, total nitrogen and their stable isotopic composition in algae and marine sediment. Rapid Commun. Mass Spectrom. 2005, 19:1063-1068.
50. Knittel K., Boetius A.O.M. Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 2009, 63:311-334.
51. Lang S.Q., Butterfield D.A., Schulte M., Kelley D.S., Lilley M.D. Elevated concentrations of formate, acetate and dissolved organic carbon found at the Lost City Hydrothermal Field. Geochim. Cosmochim. Acta 2010, 74:941-952.
52. Lartaud F., Little C.T.S., Rafelis M.D., Bayon G., Dyment J., Ildefonse B. Fossil evidence for serpentinization fluids fueling chemosynthetic assemblages. Proc. Natl. Acad. Sci. USA 2011, 108:7698-7703.
53. Londry K.L., Dawson K.G., Grover H.D., Summons R.E., Bradley A.S. Stable carbon isotope fractionation between substrates and products of Methanosarcina barkeri. Org. Geochem. 2008, 39:608-621.
54. Ludwig K.A., Kelley D.S., Butterfield D.A., Nelson B.K., Früh-Green G. Formation and evolution of carbonate chimneys at the Lost City Hydrothermal Field. Geochim. Cosmochim. Acta 2006, 70:3645-3685.
55. Ludwig K.A., Chuan-Chou S., Kelley D.S., Cheng H., Edwards R.L. U-Th systematics and 230-Th ages of carbonate chimneys at the Lost City Hydrothermal Field. Geochim. Cosmochim. Acta 2011, 75:1869-1888.
56. Martin W., Russell M.J. On the origin of biochemistry at an alkaline hydrothermal vent. Phil. Trans. R. Soc. B 2007, 362:1887-1926.
57. Martin W., Baross J., Kelley D., Russell M.J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 2008, 6:805-814.
58. McCollom T.M. Geochemical constraints on sources of metabolic energy for chemolithoautotrophy in ultramafic-hosted deep-sea hydrothermal systems. Astrobiology 2007, 7:933-950.
59. McCollom T.M., Bach W. Thermodynamic constraints on hydrogen generation during serpentinization of ultramafic rocks. Geochim. Cosmochim. Acta 2009, 73:856-875.
60. McCollom T.M., Seewald J.S. Experimental constraints on the hydrothermal reactivity of organic acids and acid anions: I. Formic acid and formate. Geochim. Cosmochim. Acta 2003, 67:3625-3644.
61. Méhay S., et al. Archaeal communities of the Lost City Hydrothermal Field. Geochim. Cosmochim. Acta Suppl. 2010, 74:A693.
62. Ménez B., Pasini V., Brunelli D. Life in the hydrated suboceanic mantle. Nat. Geosci. 2012, 5:133-137.
63. Mook W.G., Bommerso Jc., Staverma Wh. Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon-dioxide. Earth Planet. Sci. Lett. 1974, 22:169-176.
64. Neal C., Stanger G. Hydrogen generation from mantle source rocks in Oman. Earth Planet. Sci. Lett. 1983, 66:315-320.
65. Ohara Y., Reagan M.K., Fujikura K., Watanabe H., Michibayashi K., Ishii T., Stern R.J., Pujana I., Martinez F., Girard G., Ribeiro J., Brounce M., Komori N., Kino M. A serpentinite-hosted ecosystem in the Southern Mariana Forearc. Proc. Natl. Acad. Sci. USA 2012, 109:2831-2835.
66. Orphan V.J., House C.H., Hinrichs K.-U., McKeegan K.D., DeLong E.F. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl. Acad. Sci. 2002, 99:7663-7668.
67. Proskurowski G., Lilley M.D., Kelley D.S., Olson E.J. Low temperature volatile production at the Lost City Hydrothermal Field, evidence from a hydrogen stable isotope geothermometer. Chem. Geol. 2006, 229:331-343.
68. Proskurowski G., et al. Abiogenic hydrocarbon production at Lost City Hydrothermal Field. Science 2008, 319:604-607.
69. Rabus R., Hansen T.A., Widdel F. (2006) Dissimilatory sulfate- and sulfur-reducing prokaryotes. In The Prokaryotes, vol. 2 (eds. M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer and E. Stackebrandt). Singapore. pp. 659-768.
70. Reimer P.J., Brown T.A., Reimer R.W. Discussion: reporting and calibration of post-bomb C-14 data. Radiocarbon 2004, 46:1299-1304.
71. Ruff M., Wacker L., Gäggeler H.W., Suter M., Synal H.-A., Szidat S. A gas ion source for radiocarbon measurements at 200kV. Radiocarbon 2007, 2:307-314.
72. 2 in anaerobic-bacteria via a novel pathway not involving reactions of the citric-acid cycle. Arch. Microbiol. 1986, 145:162-172.
73. Schrenk M.O., Kelley D.S., Bolton S.A., Baross J.A. Low archaeal diversity linked to subseafloor geochemical processes at the Lost City Hydrothermal Field, Mid-Atlantic Ridge. Environ. Microbiol. 2004, 6:1086-1095.
74. Schulte M., Blake D., Hoehler T., McCollom T. Serpentinization and its implications for life on the early Earth and Mars. Astrobiology 2006, 6:364-376.
75. Shock E. Stability of peptides in high-temperature aqueous solutions. Geochim. Cosmochim. Acta 1992, 56:3481-3491.
76. Shock L., Schulte D. Organic synthesis during fluid mixing in hydrothermal systems. J. Geophys. Res. - Planets 1998, 103:28513-28527.
77. 2 by Desulfotomaculum Acetoxidans - demonstration of enzymes required for the operation of an oxidative acetyl-CoA carbon-monoxide dehydrogenase pathway. Arch. Microbiol. 1988, 150:374-380.
78. 2-rich fluids from serpentinization: geochemical and biotic implications. Proc. Natl. Acad. Sci. USA 2004, 101:12818-12823.
79. Sleep N.H., Bird D.K., Pope E.C. Serpentinite and the dawn of life. Phil. Trans. R. Soc. B 2011, 366:2857-2869.
80. Stams A.J.M., Plugge C.M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 2009, 7:568-577.
81. Stuiver M., Polach H.A. Discussion reporting of 14C data. Radiocarbon 1977, 19:355-363.
82. Synal H.-A., Stocker M., Suter M. MICADAS: A new compact radiocarbon AMS system. Nucl. Instrum. Methods Phys. Res. Sect. B: Beam Interact. Mater. Atoms 2007, 259:7-13.
83. Thauer, et al. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 2008, 6:576-591.
84. Von Damm K.L., Edmond J.M., Grant B., Measures C.I. Chemistry of submarine hydrothermal solutions at 21-degrees-N, East Pacific Rise. Geochim. Cosmochim. Acta 1985, 49:2197-2220.
85. Wacker L., Christl M., Synal H.A. Bats: a new tool for AMS data reduction. Nucl. Instrum. Methods Phys. Res. B 2010, 268:976-979.
86. Widdel F., Pfennig N. New Anaerobic, sporing, acetate-oxidizing, sulfate-reducing bacterium, Desulfotomaculum (emend) acetoxidans. Arch. Microbiol. 1977, 112:119-122.
87. Widdel F., Pfennig N. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty-acids. 1. Isolation of new sulfate reducing bacteria enriched with acetate from saline environments - description of Desulfobacter postgatei gen. nov. Sp. now. Arch. Microbiol. 1981, 129:395-400.