Anaerobic oxidation of methane in hypersaline Messinian environments revealed by 13C-depleted molecular fossils

Chemical Geology

Volumn 292-293, Issue , 2012, Pages 140-148

  Ziegenbalg, S B ^a,b   Birgel, D ^b   Hoffmann Sell, L ^a   Pierre, C ^c   Rouchy, J M ^d   Peckmann, J ^b  

^a UNIVERSITY OF BREMEN   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^d MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Anaerobic oxidation of methane; Authigenic carbonates; Hypersaline conditions; Lipid biomarkers; Messinian; Sicily

Indexed keywords

ANAEROBIC OXIDATION OF METHANES; AUTHIGENIC CARBONATES; HYPERSALINE CONDITIONS; LIPID BIOMARKERS; MESSINIAN; SICILY;

BACTERIA; BIODEGRADATION; BIOMARKERS; CARBONATE MINERALS; FATTY ACIDS; GLYCEROL; GYPSUM; LIMESTONE; OXIDATION; SULFUR; SULFUR COMPOUNDS;

METHANE;

ANOXIC CONDITIONS; BIODEGRADATION; BIOMARKER; CARBON ISOTOPE; CARBONATE ROCK; FOSSIL; HYPERSALINE ENVIRONMENT; LIMESTONE; LIPID; MESSINIAN; METHANE; METHANOGENIC BACTERIUM; MICROBIAL ACTIVITY; OXIDATION; SULFATE-REDUCING BACTERIUM;

APENNINES; ITALY; SICILY;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 84855358263     PISSN: 00092541     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chemgeo.2011.11.024     Document Type: Article

References (86)

1. Baudrand M., Grossi V., Pancost R., Aloisi G. Non-isoprenoid macrocyclic glycerol diethers associated with authigenic carbonates. Organic Geochemistry 2010, 41:1341-1344.
2. Birgel D., Peckmann J., Klautzsch S., Thiel V., Reitner J. Anaerobic and aerobic oxidation of methane at Late Cretaceous seeps in the Western Interior seaway, USA. Geomicrobiology Journal 2006, 23:565-577.
3. Birgel D., Thiel V., Hinrichs K.-U., Elvert M., Campbell K.A., Reitner J., Farmer J.D., Peckmann J. Lipid biomarker patterns of methane-seep microbialites from the Mesozoic convergent margin of California. Organic Geochemistry 2006, 37:1289-1302.
4. 13C-depleted biphytanic diacids as tracers of past anaerobic oxidation of methane. Organic Geochemistry 2008, 39:152-156.
5. Birgel D., Himmler T., Freiwald A., Peckmann J. A new constraint on the antiquity of anaerobic oxidation of methane: Late Pennsylvanian seep limestones from southern Namibia. Geology 2008, 36:543-546.
6. Blumenberg M., Seifert R., Reitner J., Pape T., Michaelis W. Membrane lipid patterns typify distinct anaerobic methanotrophic consortia. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:11111-11116.
7. Blumenberg M., Krüger M., Nauhaus K., Talbot H.M., Oppermann B.I., Seifert R., Pape T., Michaelis W. Biosynthesis of hopanoids by sulfate-reducing bacteria (genus Desulfovibrio). Environmental Microbiology 2006, 8:1220-1227.
8. Blumenberg M., Seifert R., Petersen S., Michaelis W. Biosignatures present in a hydrothermal massive sulfide from the Mid-Atlantic Ridge. Geobiology 2007, 5:435-450.
9. Boetius A., Ravenschlag K., Schubert C.J., Rickert D., Widdel F., Gieseke A., Amann R., Jørgensen B.B., Witte U., Pfannkuche O. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 2000, 407:623-626.
10. Böttcher M.E., Parafiniuk J. Methane-derived carbonates in a native sulphur deposit: stable isotope and trace element discriminations related to the transformation of aragonite to calcite. Isotopes in Environmental and Health Studies 1998, 34:177-190.
11. Coleman M.L., Hedrick D.B., Lovley D.R., White D.C., Pye K. Reduction of Fe (III) in sediments by sulphate-reducing bacteria. Nature 1993, 361:436-438.
12. Daffonchio D., Borin S., Brusa T., Brusetti L., van der Wielen P.W.J.J., Bolhuis H., Yakimov M.M., D'Auria G., Giuliano L., Marty D., Tamburini C., McGenity T.J., Hallsworth J.E., Sass A.M., Timmis K.N., Tselepides A., de Lange G.J., Hübner A., Thomson J., Varnavas S.P., Gasparoni F., Gerber H.W., Malinverno E., Corselli C. Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline. Nature 2006, 440:203-207. the Biodeep scientific party.
13. De Boever E., Birgel D., Thiel V., Muchez P., Peckmann J., Dimitrov L., Swennen R. The formation of giant tubular concretions triggered by anaerobic oxidation of methane as revealed by archaeal molecular fossils (Lower Eocene, Varna, Bulgaria). Palaeogeography Palaeoclimatology Palaeoecology 2009, 280:23-36.
14. De Rosa M., Gambacorta A. The lipids of archaebacteria. Progress in Lipid Research 1988, 27:153-175.
15. Decima A., Wezel F.C. Late Miocene evaporites of the central Sicilian basin, Italy. Initial Reports of the Deep Sea Drilling Project 1973, Volume 13:1234-1241. US Government Printing Office, Washington.
16. Decima A., McKenzie J.A., Schreiber B.C. The origin of "evaporative" limestones: an example from the Messinian of Sicily (Italy). Journal of Sedimentary Petrology 1988, 58:256-272.
17. Dessau G., Jensen M.L., Nakai N. Geology and isotopic studies of Sicilian sulfur deposits. Economic Geology 1962, 57:410-438.
18. Dowling N.J.E., Widdel F., White D.C. Phospholipid ester-linked fatty acid biomarkers of acetate-oxidizing sulphate-reducers and other sulphide-forming bacteria. Journal of General Microbiology 1986, 132:1815-1825.
19. Duggen S., Hoernle K., van den Bogaard P., Rüpke K., Morgan J.P. Deep roots of the Messinian salinity crisis. Nature 2003, 422:602-606.
20. Edlund A., Nichols P.D., Roffey R., White D.C. Extractable and lipopolysaccharide fatty acid and hydroxy acid profiles from Desulfovibrio species. Journal of Lipid Research 1985, 26:982-988.
21. Elvert M., Boetius A., Knittel K., Jørgensen B.B. Characterization of specific membrane fatty acids as chemotaxonomic markers for sulphate-reducing bacteria involved in anaerobic oxidation of methane. Geomicrobiology Journal 2003, 20:403-419.
22. Elvert M., Hopmans E.C., Treude T., Boetius A., Suess E. Spatial variations of methanotrophic consortia at cold methane seeps: implications from a high-resolution and isotopic approach. Geobiology 2005, 3:195-209.
23. Gasiewicz A. Comparative study of major element geochemistry of gypsum-ghost limestones and selenite lithofacies from the Miocene of northern Carpathian Foredeep: implications to the model of massive replacement of solid sulphates by calcium carbonates. Chemical Geology 2000, 164:183-218.
24. Harvey H.R., McManus G.B. Marine ciliates as a widespread source of tetrahymanol and hopan-3-beta-ol in sediments. Geochimica et Cosmochimia Acta 1991, 55:3387-3390.
25. Heindel K., Birgel D., Peckmann J., Kuhnert H., Westphal H. Formation of deglacial microbialites in coral reefs off Tahiti (IODP 310). Palaios 2010, 25:618-635.
26. 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.
27. Hinrichs K.-U., Summons R.E., Orphan V., Sylva S.P., Hayes J.M. Molecular and isotopic analysis of anaerobic methane-oxidizing communities in marine sediments. Organic Geochemistry 2000, 31:1685-1701.
28. Holler T., Widdel F., Knittel K., Amann R., Kellermann M.Y., Hinrichs K.-U., Teske A., Boetius A., Wegener G. Thermophilic anaerobic oxidation of methane by marine microbial consortia. The ISME Journal 2011, 5:1946-1956.
29. Holzer G., Oró J., Tornabene T.G. Gas chromatographic-mass spectrometric analysis of neutral lipids from methanogenic and thermoacidophilic bacteria. Journal of Chromatography A 1979, 186:795-809.
30. Hsü K.J., Cita M.B., Ryan W.B.F. The origin of the Mediterranean evaporites. Initial Reports of the Deep Sea Drilling Projects 1973, Volume 13:1203-1231. US Government Printing Office, Washington.
31. Hsü K.J., Ryan W.B.F., Cita M.B. Late Miocene desiccation of the Mediterranean. Nature 1973, 424:240-244.
32. Huguen C., Foucher J.P., Mascle J., Ondréas H., Thouement M., Gontharet S., Stadnitskaia A., Pierre C., Bayon G., Loncke L., Boetius A., Bouloubassi I., de Lange G. Menes caldera, a highly active site of brine seepage in the Eastern Mediterranean sea: "in situ" observations from the NAUTINIL expedition (2003). Marine Geology 2009, 261:138-152. the NAUTINIL scientific party.
33. Joye S.B., Samarkin V.A., Orcutt B.N., MacDonald I.R., Hinrichs K.-U., Elvert M., Teske A.P., Lloyd K.G., Lever M.A., Montoya J.P., Meile C.D. Metabolic variability in seafloor brines revealed by carbon and sulphur dynamics. Nature Geoscience 2009, 2:349-354.
34. Kates M. Membrane lipids of extreme halophiles: biosynthesis, function and evolutionary significance. Experientia 1993, 49:1027-1036.
35. Kemp P., Lander D.J., Orpin C.G. The lipids of the rumen fungus Piromonas communis. Journal of General Microbiology 1984, 130:27-37.
36. Kirkland D.W., Evans R. Origin of limestone buttes, Gypsum Plain, Culberson County, Texas. American Association of Petroleum Geologists Bulletin 1976, 60:2005-2018.
37. Kleemann G., Poralla K., Englert G., Kjosen H., Liaaen-Jensen S., Neunlist S., Rohmer M. Tetrahymanol from the phototrophic bacterium Rhodopseudomonas palustris: first report of a gammacerane triterpene from a prokaryote. Journal of General Microbiology 1990, 136:2551-2553.
38. Knittel K., Boetius A., Lemke A., Eilers H., Lochte K., Pfannkuche O., Linke P., Amann R. Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia Margin, Oregon). Geomicrobiology Journal 2003, 20:269-294.
39. Koga Y., Nishihara M., Morii H., Akagawa-Matsushita M. Ether polar lipids of methanogenic bacteria: structures, comparative aspects, and biosyntheses. Microbiological Reviews 1993, 57:164-182.
40. Koga Y., Morii H., Akagawa-Matsuchita M., Ohga M. Correlation of polar lipid composition with 16S rRNA phylogeny in methanogens. Further analysis of lipid component parts. Bioscience Biotechnology Biochemistry 1998, 62:230-236.
41. Könneke M., Widdel F. Effect of growth temperature on cellular fatty acids in sulphate-reducing bacteria. Environmental Microbiology 2003, 5:1064-1070.
42. Krijgsman W., Hilgen F.J., Raffi I., Sierro F.J., Wilson D.S. Chronology, causes and progression of the Messinian salinity crisis. Nature 1999, 400:652-655.
43. Lindtke J., Ziegenbalg S.B., Brunner B., Rouchy J.M., Pierre C., Peckmann J. Authigenesis of native sulphur and dolomite in a lacustrine evaporitic setting (Hellín basin, Late Miocene, SE Spain). Geological Magazine 2011, 148:655-669.
44. Londry K.L., Jahnke L.L., Marais D.J.D. Stable carbon isotope ratios of lipid biomarkers of sulfate-reducing bacteria. Applied and Environmental Microbiology 2004, 70:745-751.
45. McKenzie J.A. Holocene dolomitization of calcium carbonate sediments from the coastal sabkhas of Abu Dhabi, U.A.E.: a stable isotope study. Journal of Geology 1981, 89:185-198.
46. Michaelis W., Seifert R., Nauhaus K., Treude T., Thiel V., Blumenberg M., Knittel K., Gieseke A., Peterknecht K., Pape T., Boetius A., Amann R., Jørgensen B.B., Widdel F., Peckmann J., Pimenov N.V., Maksim G.B. Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 2002, 297:1013-1015.
47. Niederberger T.D., Perreault N.N., Tille S., Lollar B.S., Lacrampe-Couloume G., Andersen D., Greer C.W., Pollard W., Whyte L.G. Microbial characterization of a subzero, hypersaline methane seep in the Canadian High Arctic. International Society for Microbial Ecology Journal 2010, 4:1326-1339.
48. Niemann H., Elvert M. Diagnostic lipid biomarkers and stable carbon isotope signatures of microbial communities mediating the anaerobic oxidation of methane with sulphate. Organic Geochemistry 2008, 39:1668-1677.
49. Oba M., Sakata S., Tsunogai U. Polar and neutral isopranyl glycerol ether lipids as biomarkers of archaea in near-surface sediments from the Nankai Trough. Organic Geochemistry 2006, 37:1643-1654.
50. Omoregie E.O., Niemann H., Mastalerz V., de Lange G.J., Stadnitskaia A., Mascle J., Foucher J.-P., Boetius A. Microbial methane oxidation and sulfate reduction at cold seeps of the deep Eastern Mediterranean Sea. Marine Geology 2009, 261:114-127.
51. Orphan V.J., Hinrichs K.-U., Ussler W., Paull C.K., Taylor L.T., Sylva S.P., Hayes J.M., DeLong E.F. Comparative analysis of methane-oxidizing archaea and sulphate-reducing bacteria in anoxic marine sediments. Applied and Environmental Microbiology 2001, 67:1922-1934.
52. Orphan V.J., House C.H., Hinrichs K.-U., McKeegan K.D., DeLong E.F. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 2001, 293:484-487.
53. 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. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:7663-7668.
54. Pancost R.D., Sinninghe Damsté J.S., de Lint S., van der Maarel M.J.E.C., Gottschal J.C. Biomarker evidence for widespread anaerobic methane oxidation in Mediterranean sediments by a consortium of methanogenic archaea and bacteria. Applied and Environmental Microbiology 2000, 66:1126-1132. the MEDINAUT shipboard scientific party.
55. Pancost R.D., Bouloubassi I., Aloisi G., Sinninghe Damsté J.S. Three series of non-isoprenoidal dialkyl glycerol diethers in cold-seep carbonate crusts. Organic Geochemistry 2001, 32:695-707. the Medinaut Shipboard Scientific Party.
56. Pancost R.D., Hopmans E.C., Sinninghe Damsté J.S. Archaeal lipids in Mediterranean cold seeps: molecular proxies for anaerobic methane oxidation. Geochimica et Cosmochimica Acta 2001, 65:1611-1627. the MEDINAUT shipboard scientific party.
57. Pancost R.D., Pressley S., Coleman J.M., Talbot H.M., Kelly S.P., Farrimond P., Schouten S., Benning L., Mountain B.W. Composition and implications of diverse lipids in New Zealand Geothermal sinters. Geobiology 2006, 4:71-92.
58. Pape T., Blumenberg M., Seifert R., Egorov V.N., Gulin S.B., Michaelis W. Lipid geochemistry of methane-seep-related Black Sea carbonates. Palaeogeography Palaeoclimatology Palaeoecology 2005, 227:31-47.
59. Peckmann J., Thiel V. Carbon cycling at ancient methane-seeps. Chemical Geology 2004, 205:443-467.
60. Peckmann J., Paul J., Thiel V. Bacterially mediated formation of diagenetic aragonite and native sulfur in Zechstein carbonates (Upper Permian, Central Germany). Sedimentary Geology 1999, 126:205-222.
61. Peckmann J., Thiel V., Michaelis W., Clari P., Gaillard C., Martire L., Reitner J. Cold seep deposits of Beauvoisin (Oxfordian; southeastern France) and Marmorito (Miocene, northern Italy): microbially induced authigenic carbonates. International Journal of Earth Sciences 1999, 88:60-75.
62. Peckmann J., Birgel D., Kiel S. Molecular fossils reveal fluid composition and flow intensity at a Cretaceous seep. Geology 2009, 37:847-850.
63. Rashby S.E., Sessions A.L., Summons R.E., Newman D.K. Biosynthesis of 2-methylbacteriohopanepolyols by an anoxygenic phototroph. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:15099-15104.
64. Rouchy J.M., Caruso A. The Messinian salinity crisis in the Mediterranean basin: a reassessment of the data and an integrated scenario. Sedimentary Geology 2006, 188-189:35-67.
65. Roveri M., Lugli S., Manzi V., Gennari R., Iaccarino S.M., Grossi F., Taviani M. Field-trip itinerary. The record of Messinian events in the northern Apennines foredeep basins, R.C.M.N.S. Interim colloquium 'The Messinian salinity crisis revisited-II', Pre-congress field-trip. Acta naturalia de "L'Ateneo Parmense" 42, Parma 2006, 38-65. M. Roveri, S. Lugli, V. Manzi, R. Gennari, S.M. Iaccarino, F. Grossi, M. Taviani (Eds.).
66. Rütters H., Sass H., Cypionka H., Rullkötter J. Monoalkylether phospholipids in the sulfate-reducing bacteria Desulfosarcina variabilis and Desulforhabdus amnigenus. Archives of Microbiology 2001, 176:435-442.
67. Rütters H., Sass H., Cypionka H., Rullkötter J. Phospholipid analysis as a tool to study complex microbial communities in marine sediments. Journal of Microbiological Methods 2002, 48:149-160.
68. Schouten S., Wakeham S.G., Hopmans E.C., Sinninghe Damsté J.S. Biogeochemical evidence that thermophilic archaea mediate the anaerobic oxidation of methane. Applied and Environmental Microbiology 2003, 69:1680-1686.
69. 16 ratios of total oxygen of carbonates. Geochimica et Cosmochimica Acta 1965, 29:1347-1353.
70. Sprott G.D. Structures of archaebacterial membrane-lipids. Journal of Bioenergetics and Biomembranes 1992, 24:555-566.
71. Sprott G.D., Ekiel I., Dicaire D. Novel, acid-labile, hydroxydiether lipid cores in methanogenic bacteria. Journal of Biological Chemistry 1990, 265:13735-13740.
72. Sprott G.D., Dicaire C.J., Choquet C.G., Patel G.B., Ekiel I. Hydroxydiether lipid structures in Methanosarcina spp. and Methanococcus voltae. Applied and Environmental Microbiology 1993, 59:912-914.
73. Stadnitskaia A., Muyzer G., Abbas B., Coolen M.J.L., Hopmans E.C., Baas M., van Weering T.C.E., Ivanov M.K., Poludetkina E., Sinninghe Damsté J.S. Biomarker and 16S rDNA evidence for anaerobic oxidation of methane and related carbonate precipitation in deep-sea mud volcanoes of the Sorokin Through, Black Sea. Marine Geology 2005, 217:67-96.
74. Taylor J., Parkes R.J. The cellular fatty acids of the sulphate-reducing bacteria, Desulfobacter sp., Desulfolobus sp. and Desulfovibrio desulfuricans. Journal of General Microbiology 1983, 129:3303-3309.
75. Teixidor P., Grimalt J.O., Pueyo J.O., Rodriguez-Valera F. Isopranylglycerol diethers in non-alkaline evaporitic environments. Geochimica et Cosmochimica Acta 1993, 57:4479-4489.
76. ten Haven H.L., de Leeuw J.W., Sinninghe Damsté J.S., Schenck P.A., Palmer S.E., Zumberge J.E. Application of biological markers in the recognition of palaeo-hypersaline environments. Lacustrine petroleum source rocks. Geological Society Special Publication No. 40 1988, 123-130. A.J. Fleet, M.R. Talbot (Eds.).
77. ten Haven H.L., Rohmer M., Rullkötter J., Bisseret P. Tetrahymanol, the most likely precursor of gammacerane, occurs ubiquitously in marine sediments. Geochimica et Cosmochimica Acta 1989, 53:3073-3079.
78. Thiel V., Peckmann J., Seifert R., Wehrung P., Reitner J., Michaelis W. Highly isotopically depleted isoprenoids: Molecular markers for ancient methane venting. Geochimica et Cosmochimica Acta 1999, 63:3959-3966.
79. Thiel V., Peckmann J., Richnow H.H., Luth U., Reitner J., Michaelis W. Molecular signals for anaerobic methane oxidation in Black Sea seep carbonates and a microbial mat. Marine Chemistry 2001, 73:97-112.
80. Thiel V., Blumenberg M., Pape T., Seifert R., Michaelis W. Unexpected occurrence of hopanoids at gas seeps in the Black Sea. Organic Geochemistry 2003, 34:81-87.
81. Tornabene T.G., Langworthy T.A. Diphytanyl and dibiphytanyl glycerol ether lipids of methanogenic archaebacteria. Science 1979, 203:51-53.
82. Wankel S.D., Joye S.B., Samarkin V.A., Shah S.R., Friederich G., Melas-Kyriazi J., Girguis P.R. New constraints on methane fluxes and rates of anaerobic methane oxidation in a Gulf of Mexico brine pool via in situ mass spectrometry. Deep-Sea Research II 2010, 57:2022-2029.
83. 25 isoprenoid hydrocarbon in Tertiary sediments representing a lagoonal-type, saline environment. Geochimica et Cosmochimica Acta 1974, 38:381-387.
84. Werne J.P., Baas M., Sinninghe Damsté J.S. Molecular isotopic tracing of carbon flow and trophic relationships in a methane-supported benthic microbial community. Limnology and Oceanography 2002, 47:1694-1701.
85. Zander J.M., Caspi E., Pandey G.N., Mitra C.R. The presence of tetrahymanol in Oleandra wallichii. Phytochemistry 1969, 8:2265-2267.
86. Ziegenbalg S.B., Brunner B., Rouchy J.M., Birgel D., Pierre C., Böttcher M.E., Caruso A., Immenhauser A., Peckmann J. Formation of secondary carbonates and native sulphur in sulphate-rich Messinian strata, Sicily. Sedimentary Geology 2010, 227:37-50.