Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids in the Arabian Sea oxygen minimum zone. Part II: Selective preservation and degradation in sediments and consequences for the TEX86

Geochimica et Cosmochimica Acta

Volumn 98, Issue , 2012, Pages 244-258

  Lengger, Sabine K ^a   Hopmans, Ellen C ^a   Reichart, Gert Jan ^b   Nierop, Klaas G J ^b   Sinninghe Damsté, Jaap S ^a,b   Schouten, Stefan ^a,b  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CONCENTRATION (COMPOSITION); DEGRADATION; ETHER; LIPID; MARINE SEDIMENT; OXYGEN; PHOSPHOLIPID; REDOX CONDITIONS; SEDIMENT CORE;

ARABIAN SEA; INDIAN OCEAN;

ARCHAEA;

EID: 84875500351     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2012.05.003     Document Type: Article

References (93)

1. Abell G.C.J., Banks J., Ross D.J., Keane J.P., Robert S.S., Revill A.T., Volkman J.K. Effects of estuarine sediment hypoxia on nitrogen fluxes and ammonia oxidizer gene transcription. FEMS Microbiol. Ecol. 2011, 75:111-122.
2. Agogué H., Brink M., Dinasquet J., Herndl G.J. Major gradients inputatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 2008, 456:788-791.
3. Beman J.M., Francis C.A. Diversity of ammonia-oxidizing Archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahía del Tóbari, Mexico. Appl. Environ. Microbiol. 2006, 72:7767-7777.
4. Biddle J.F., Lipp J.S., Lever M.A., Lloyd K.G., Sørensen K.B., Anderson R., Fredricks H.F., Elvert M., Kelly T.J., Schrag D.P., Sogin M.L., Brenchley J.E., Teske A., House C.H., Hinrichs K.-U. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc. Natl. Acad. Sci. USA 2006, 103:3846-3851.
5. Bijl P.K., Schouten S., Sluijs A., Reichart G.-J., Zachos J.C., Brinkhuis H. Early Palaeogene temperature evolution of the southwest Pacific Ocean. Nature 2009, 461:776-779.
6. Brochier-Armanet C., Boussau B., Gribaldo S., Forterre P. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 2008, 6:245-252.
7. Caffrey J.M., Bano N., Kalanetra K., Hollibaugh J.T. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. Int. Soc. Microb. Ecol. 2007, 1:660-662.
8. Cavicchioli R. Cold-adapted archaea. Nat. Rev. Microbiol. 2006, 4:331-343.
9. Chen X.-P., Zhu Y.-G., Xia Y., Shen J.-P., He J.-Z. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil?. Environ. Microbiol. 2008, 10:1978-1987.
10. Coolen M.J.L., Abbas B., van Bleijswijk J., Hopmans E.C., Kuypers M.M.M., Wakeham S.G., Sinninghe Damsté J.S. Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids. Environ. Microbiol. 2007, 9:1001-1016.
11. de la Torre J.R., Walker C.B., Ingalls A.E., Könneke M., Stahl D.A. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 2008, 10:810-818.
12. de Rosa M., Gambacorta A. The lipids of archaebacteria. Prog. Lipid Res. 1988, 27:153-175.
13. DeLong E.F. Archaea in coastal marine environments. Proc. Natl. Acad. Sci. USA 1992, 89:5685-5689.
14. DeLong E.F., King L.L., Massana R., Cittone H., Murray A., Schleper C., Wakeham S.G. Dibiphytanyl ether lipids in nonthermophilic Crenarchaeotes. Appl. Environ. Microbiol. 1998, 64:1133-1138.
15. Erguder T.H., Boon N., Wittebolle L., Marzorati M., Verstraete W. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol. Rev. 2009, 33:855-869.
16. Forster A., Schouten S., Baas M., Sinninghe Damsté J.S. Mid-Cretaceous (Albian-Santonian) sea surface temperature record of the tropical Atlantic Ocean. Geology 2007, 35:919-922.
17. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., Oakley B.B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. USA 2005, 102:14683-14688.
18. Fuhrman J.A., McCallum K., Davies A.A. Novel major archaebacterial group from marine plankton. Nature 1992, 356:148-149.
19. Gabriel J.L., Chong P.L.G. Molecular modeling of archaebacterial bipolar tetraether lipid membranes. Chem. Phys. Lipids 2000, 105:193-200.
20. Gliozzi A., Rolandi R., de Rosa M., Gambacorta A. Monolayer black membranes from bipolar lipids of archaebacteria and their temperature-induced structural changes. J. Membr. Biol. 1983, 75:45-56.
21. Harvey H.R., Fallon R.D., Patton J.S. The effect of organic matter and oxygen on the degradation of bacterial membrane lipids in marine sediments. Geochim. Cosmochim. Acta 1986, 50:795-804.
22. Hatzenpichler R., Lebedeva E.V., Spieck E., Stoecker K., Richter A., Daims H., Wagner M. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA 2008, 105:2134-2139.
23. Hedges J.I., Keil R.G. Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar. Chem. 1995, 49:81-115.
24. Herndl G.J., Reinthaler T., Teira E., van Aken H., Veth C., Pernthaler A., Pernthaler J. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl. Environ. Microbiol. 2005, 71:2303-2309.
25. Hoefs M.J.L., Rijpstra W.I.C., Sinninghe Damsté J.S. The influence of oxic degradation on the sedimentary biomarker record I: evidence from Madeira Abyssal Plain turbidites. Geochim. Cosmochim. Acta 2002, 66:2719-2735.
26. Huguet C., Cartes J.E., Sinninghe Damsté J.S., Schouten S. Marine crenarchaeotal membrane lipids in decapods: implications for the TEX86 paleothermometer. Geochem. Geophys. Geosyst. 2006, 7:1-12.
27. Huguet C., Hopmans E.C., Febo-Ayala W., Thompson D.H., Sinninghe Damsté J.S., Schouten S. An improved method to determine the absolute abundance of glycerol dibiphytanyl glycerol tetraether lipids. Org. Geochem. 2006, 37:1036-1041.
28. K'37). Paleoceanography 2006, 21. PA3003.
29. Huguet C., Schimmelmann A., Thunell R., Lourens L.J., Sinninghe Damsté J.S., Schouten S. A study of the TEX86 paleothermometer in the water column and sediments of the Santa Barbara Basin, California. Paleoceanography 2007, 22. PA3203.
30. Huguet C., de Lange G.J., Gustafsson Ö., Middelburg J.J., Sinninghe Damsté J.S., Schouten S. Selective preservation of soil organic matter in oxidized marine sediments (Madeira Abyssal Plain). Geochim. Cosmochim. Acta 2008, 72:6061-6068.
31. Huguet C., Urakawa H., Martens-Habbena W., Truxal L., Stahl D.A., Ingalls A.E. Changes in intact membrane lipid content of archaeal cells as an indication of metabolic status. Org. Geochem. 2010, 41:930-934.
32. Ingalls A.E., Shah S.R., Hansman R.L., Aluwihare L.I., Santos G.M., Druffel E.R.M., Pearson A. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Natl. Acad. Sci. USA 2006, 103:6442-6447.
33. Jensen M.M., Lam P., Revsbech N.P., Nagel B., Gaye B., Jetten M.S.M., Kuypers M.M.M. Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. Int. Soc. Microb. Ecol. 2011, 5:1660-1670.
34. Karner M.B., DeLong E.F., Karl D.M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 2001, 409:507-510.
35. Kates M., Yengoyan L.S., Sastry G.N. A diether analog of phosphatidyl glycerophosphate in Halobacterium cutirubrum. Biochim. Biophys. Acta 1965, 98:252-268.
36. 86 paleothermometer in the ocean. Geochim. Cosmochim. Acta 2008, 72:1154-1173.
37. Kim J.-H., van der Meer J., Schouten S., Helmke P., Willmott V., Sangiorgi F., Koç N., Hopmans E.C., Sinninghe Damsté J.S. New indices and calibrations derived from the distribution of crenarchaeal isoprenoid tetraether lipids: implications for past sea surface temperature reconstructions. Geochim. Cosmochim. Acta. 2010, 74:4639-4654.
38. Koga Y., Morii H. Recent advances in structural research on ether lipids from archaea including comparative and physiological aspects. Biosci. Biotechnol. Biochem. 2005, 69:2019-2034.
39. Koga Y., Nakano M. A dendrogram of archaea based on lipid component parts composition and its relationship to rRNA phylogeny. Syst. Appl. Microbiol. 2008, 31:169-182.
40. Könneke M., Bernhard A.E., de la Torre J.R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
41. Kraal P., Slomp C.P., Reed D.C., Reichart G.J., Poulton S.W. Sedimentary phosphorus and iron cycling in and below the oxygen minimum zone of the Northern Arabian Sea. Biogeosci. Discuss. 2012, 9:3829-3880.
42. Kuypers M.M.M., Blokker P., Erbacher J., Kinkel H., Pancost R.D., Schouten S., Sinninghe Damsté J.S. Massive expansion of marine archaea during a mid-cretaceous oceanic anoxic event. Science 2001, 293:92-94.
43. Langworthy T.A., Smith P.F., Mayberry W.R. Lipids of Thermoplasma acidophilum. J. Bacteriol. 1972, 112:1193-1200.
44. Langworthy T.A., Mayberry W.R., Smith P.F. Long-chain glycerol diether and polyol dialkyl glycerol triether lipids of Sulfolobus acidocaldarius. J. Bacteriol. 1974, 119:106-116.
45. Lebaron P., Servais P., Agogué H., Courties C., Joux F. Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems?. Appl. Environ. Microbiol. 2001, 67:1775-1782.
46. Leininger S., Urich T., Schloter M., Schwark L., Qi J., Nicol G.W., Prosser J.I., Schuster S.C., Schleper C. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 2006, 442:806-809.
47. Lengger S.K., Hopmans E.C., Sinninghe Damsté J.S., Schouten S. A comparison of extraction and work-up techniques for analysis of core- and intact polar tetraether lipids in marine sediments. Org. Geochem. 2012, 47:34-40.
48. Lipp J.S., Hinrichs K.-U. Structural diversity and fate of intact polar lipids in marine sediments. Geochim. Cosmochim. Acta 2009, 73:6816-6833.
49. Lipp J.S., Morono Y., Inagaki F., Hinrichs K.-U. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 2008, 454:991-994.
50. Liu Z., Pagani M., Zinniker D., DeConto R., Huber M., Brinkhuis H., Shah S.R., Leckie R.M., Pearson A. Global cooling during the Eocene-Oligocene climate transition. Science 2009, 323:1187-1189.
51. Liu X., Lipp J.S., Hinrichs K.-U. Distribution of intact and core GDGTs in marine sediments. Org. Geochem. 2011, 42:368-375.
52. Lopes dos Santos R.A., Prange M., Castañeda I.S., Schefuß E., Mulitza S., Schulz M., Niedermeyer E.M., Sinninghe Damsté J.S., Schouten S. Glacial-interglacial variability in Atlantic meridional overturning circulation and thermocline adjustments in the tropical North Atlantic. Earth Planet. Sci. Lett. 2010, 300:407-414.
53. Luna G.M., Manini E., Danovaro R. Large fraction of dead and inactive bacteria in coastal marine sediments: comparison of protocols for determination and ecological significance. Appl. Environ. Microbiol. 2002, 68:3509-3513.
54. Macalady J.L., Vestling M.M., Baumler D., Boekelheide N., Kaspar C.W., Banfield J.F. Tetraether-linked membrane monolayers in Ferroplasma spp a key to survival in acid. Extremophiles 2004, 8:411-419.
55. Mayer L.M. Surface area control of organic carbon accumulation in continental shelf sediments. Geochim. Cosmochim. Acta 1994, 58:1271-1284.
56. Mayer L.M., Schick L.L., Hardy K.R., Wagai R., McCarthy J. Organic matter in small mesopores in sediments and soils. Geochim. Cosmochim. Acta 2004, 68:3863-3872.
57. Oba M., Sakata S., Tsunogai U. Polar and neutral isopranyl glycerol ether lipids as biomarkers of archaea in near-surface sediments from the Nankai. Org. Geochem. 2006, 37:1643-1654.
58. Olson D.B., Hitchcock G.L., Fine R.A., Warren B.A. Maintenance of the low-oxygen layer in the central Arabian Sea. Deep Sea Res. Part II 1993, 40:673-685.
59. Pancost R.D., Hopmans E.C., Sinninghe Damsté J.S., the Medinaut Shipboard Scientific Party Archaeal lipids in Mediterranean Cold Seeps: molecular proxies for anaerobic methane oxidation. Geochim. Cosmochim. Acta 2001, 65:1611-1627.
60. Park S.-J., Park B.-J., Rhee S.-K. Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 2008, 12:605-615.
61. Park B.-J., Park S.-J., Yoon D.-N., Schouten S., Sinninghe Damsté J.S., Rhee S.-K. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl. Environ. Microbiol. 2010, 76:7575-7587.
62. Paulmier A., Ruiz-Pino D. Oxygen minimum zones (OMZs) in the modern ocean. Prog. Oceanogr. 2009, 80:113-128.
63. 14C analysis. Geochim. Cosmochim. Acta 2001, 65:3123-3137.
64. Pitcher A., Hopmans E.C., Schouten S., Sinninghe Damsté J.S. Separation of core and intact polar archaeal tetraether lipids using silica columns: insights into living and fossil biomass contributions. Org. Geochem. 2009, 40:12-19.
65. Pitcher A., Rychlik N., Hopmans E.C., Spieck E., Rijpstra W.I.C., Ossebaar J., Schouten S., Wagner M., Sinninghe Damsté J.S. Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic Group I.1b Archaeon. Int. Soc. Microb. Ecol. 2010, 4:542-552.
66. Pitcher A., Hopmans E.C., Villanueva L., Reichart G.-J., Schouten S., Sinninghe Damsté J.S. Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J. 2011, 5:1896-1904.
67. Pitcher A., Hopmans E.C., Mosier A.C., Park S.-J., Rhee S.-K., Francis C.A., Schouten S., Sinninghe Damsté J.S. Core and intact polar glycerol dibiphytanyl glycerol tetraether lipids of ammonia-oxidizing archaea enriched from marine and estuarine sediments. Appl. Environ. Microbiol. 2011, 77:3468-3477.
68. Prahl F.G., de Lange G.J., Scholten S., Cowie G.L. A case of post-depositional aerobic degradation of terrestrial organic matter in turbidite deposits from the Madeira Abyssal Plain. Org. Geochem. 1997, 27:141-152.
69. Revsbech N.P. An oxygen microsensor with a guard cathode. Limnol. Oceanogr. 1989, 34:474-478.
70. Revsbech N.P., Larsen L.H., Gundersen J., Dalsgaard T., Ulloa O., Thamdrup B. Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnol. Oceanogr. Methods 2009, 7:371-381.
71. Schleper C., Holben W., Klenk H.-P. Recovery of crenarchaeotal ribosomal DNA sequences from freshwater-lake sediments. Appl. Environ. Microbiol. 1997, 63:321-323.
72. Schouten S., Hopmans E.C., Pancost R.D., Sinninghe Damsté J.S. Widespread occurrence of structurally diverse tetraether membrane lipids: evidence for the ubiquitous presence of low-temperature relatives of hyperthermophiles. Proc. Natl. Acad. Sci. USA 2000, 97:14421-14426.
73. Schouten S., Hopmans E.C., Schefuß E., Sinninghe Damsté J.S. Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures?. Earth Planet. Sci. Lett. 2002, 204:265-274.
74. 86 palaeothermometer for tropical sea surface temperatures in ancient greenhouse worlds. Org. Geochem. 2007, 38:1537-1546.
75. Schouten S., Hopmans E.C., Baas M., Boumann H., Standfest S., Könneke M., Stahl D.A., Sinninghe Damsté J.S. Intact membrane lipids of "Candidatus Nitrosopumilus maritimus", a cultivated representative of the cosmopolitan mesophilic group I crenarchaeota. Appl. Environ. Microbiol. 2008, 74:2433-2440.
76. Schouten S., Middelburg J.J., Hopmans E.C., Sinninghe Damsté J.S. Fossilization and degradation of intact polar lipids in deep subsurface sediments: a theoretical approach. Geochim. Cosmochim. Acta 2010, 74:3806-3814.
77. 86. Geochim. Cosmochim. Acta 2012, 98:228-243.
78. Schubotz F., Wakeham S.G., Lipp J.S., Fredricks H.F., Hinrichs K.-U. Detection of microbial biomass by intact polar membrane lipid analysis in the water column and surface sediments of the Black Sea. Environ. Microbiol. 2009, 11:2720-2734.
79. Shah S.R., Mollenhauer G., Ohkouchi N., Eglinton T., Pearson A. Origins of archaeal tetraether lipids in sediments: insights from radiocarbon analysis. Geochim. Cosmochim. Acta 2008, 72:4577-4594.
80. Sinninghe Damsté J.S., Rijpstra W.I.C., Reichart G.-J. The influence of oxic degradation on the sedimentary biomarker record II. Evidence from Arabian Sea sediments. Geochim. Cosmochim. Acta 2002, 66:2737-2754.
81. Sinninghe Damsté J.S., Schouten S., Hopmans E.C., van Duin A.C.T., Geenevasen J.A.J. Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J. Lipid Res. 2002, 43:1641-1651.
82. Spang A., Hatzenpichler R., Brochier-Armanet C., Rattei T., Tischler P., Spieck E., Streit W., Stahl D.A., Wagner M., Schleper C. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 2010, 18:331-340.
83. Stevenson P.L. A case for bacterial dormancy in aquatic systems. Microb. Ecol. 1978, 4:127-133.
84. Sturt H.F., Summons R.E., Smith K., Elvert M., Hinrichs K.-U. Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry - new biomarkers for biogeochemistry and microbial ecology. Rapid Commun. Mass Spectrom. 2004, 18:617-628.
85. van der Weijden C.H., Reichart G.-J., Visser H.J. Enhanced preservation of organic matter in sediments deposited within the oxygen minimum zone in the northeastern Arabian Sea. Deep Sea Res. Part I 1999, 46:807-830.
86. Wakeham S.G., Lewis C.M., Hopmans E.C., Schouten S., Sinninghe Damsté J.S. Archaea mediate anaerobic oxidation of methane in deep euxinic waters of the Black Sea. Geochim. Cosmochim. Acta 2003, 67:1359-1374.
87. Weijers J.W.H., Lim K.L., Aquilina A., Sinninghe Damsté J.S., Pancost R.D. Biogeochemical controls on glycerol dialkyl glycerol tetraether lipid distributions in sediments characterized by diffusive methane flux. Geochem. Geophys. Geosyst. 2011, 12:Q10010.
88. Wuchter C., Schouten S., Coolen M.J.L., Sinninghe Damsté J.S. Temperature-dependent variation in the distribution of tetraether membrane lipids of marine Crenarchaeota: implications for TEX86 paleothermometry. Paleoceanography 2004, 19. PA4028.
89. Wuchter C., Schouten S., Wakeham S.G., Sinninghe Damsté J.S. Temporal and spatial variation in tetraether membrane lipids of marine Crenarchaeota in particulate organic matter: implications for TEX86 paleothermometry. Paleoceanography 2005, 20. PA3013-1-PA3013-11.
90. Wuchter C., Schouten S., Wakeham S.G., Sinninghe Damsté J.S. Archaeal tetraether membrane lipid fluxes in the northeastern Pacific and the Arabian Sea: implications for TEX86 paleothermometry. Paleoceanography 2006, 21. PA4208.
91. Wyrtki K. Oceanographic Atlas of the International Indian Ocean Expedition 1971, USGPO, Washington.
92. Wyrtki K. Physical geography of the Indian Ocean. The Biology of the Indian Ocean 1973, 18-36. Springer, Berlin.
93. Zink K.-G., Wilkes H., Disko U., Elvert M., Horsfield B. Intact phospholipids - microbial "life markers" in marine deep subsurface sediments. Org. Geochem. 2003, 34:755-769.