Assessing production of the ubiquitous archaeal diglycosyl tetraether lipids in marine subsurface sediment using intramolecular stable isotope probing

Environmental Microbiology

Volumn 15, Issue 5, 2013, Pages 1634-1646

  Lin, Yu Shih ^a   Lipp, Julius S ^a   Elvert, Marcus ^a   Holler, Thomas ^b   Hinrichs, Kai Uwe ^a  

^a UNIVERSITY OF BREMEN   (Germany)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; CARBON; GLYCEROL; LIPID; MEMBRANE LIPID; METHANE;

ARCHAEON; ARTICLE; BACTERIUM; BIOSYNTHESIS; CHEMISTRY; ENVIRONMENTAL MONITORING; METABOLISM; MICROBIOLOGY; SEDIMENT;

ARCHAEA; BACTERIA; CARBOHYDRATES; CARBON; CARBON ISOTOPES; ENVIRONMENTAL MONITORING; GEOLOGIC SEDIMENTS; GLYCEROL; LIPIDS; MEMBRANE LIPIDS; METHANE;

ARCHAEA; SPIRULINA PLATENSIS;

EID: 84876487837     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02888.x     Document Type: Article

References (41)

1. Batzke, A., Engelen, B., Sass, H., and Cypionka, H. (2007) Phylogenetic and physiological diversity of cultured deep-biosphere bacteria from Equatorial Pacific Ocean and Peru Margin sediments. Geomicrobiol J 24: 261-273.
2. Biddle, J.F., Lipp, J.S., Lever, M.A., Lloyd, K.G., Sørensen, K.B., Anderson, R., etal. (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA 103: 3846-3851.
3. Blumenberg, M., Seifert, R., Nauhaus, K., Paper, T., and Michaelis, W. (2005) In vitro study of lipid biosynthesis in an anaerobically mathane-oxidizing microbial mat. Appl Environ Microbiol 71: 4345-4351.
4. 13C-labeling of biomarkers. Nature 392: 801-805.
5. Guerrant, G.O., and Moss, C.W. (1984) Determination of monosaccharides as aldononitrile, O-methyloxime, alditol, and cyclitol acetate derivatives by gas chromatography. Anal Chem 56: 633-638.
6. Harvey, H.R., Fallon, R.D., and Patton, J.S. (1986) The effect of organic matter and oxygen on the degradation of bacterial membrane lipids in marine sediments. Geochim Cosmochim Acta 50: 795-804.
7. Hudson, B.J.F., and Karis, I.G. (1974) The lipids of the alga Spirulina. J Sci Food Agric 25: 759-763.
8. Jahn, U., Summons, R., Sturt, H., Grosjean, E., and Huber, H. (2004) Composition of the lipids of Nanoaechaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I. Arch Microbiol 182: 404-413.
9. Karner, M.B., DeLong, E.F., and Karl, D.M. (2000) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507-510.
10. Koga, Y., and Morii, H. (2005) Recent advances in structural research on ether lipids from Archaea including comparative and physiological aspects. Biosci Biotechnol Biochem 69: 2019-2034.
11. Könneke, M., Lipp, J.S., and Hinrichs, K.U. (2012) Carbon isotope fractionation by the marine ammonia-oxidizing archaeon Nitrosopumilus maritimus. Org Geochem 48: 21-24.
12. Lam, P., Jensen, M.M., Lavik, G., McGinnis, D.F., Müller, B., Schubert, C.J., etal. (2007) Linking crenarchaeol and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 104: 7104-7109.
13. Lin, Y.S., Biddle, J.F., Lipp, J.S., Orcutt, B.N., Holler, T., Teske, A., and Hinrichs, K.U. (2010a) Effect of storage conditions on archaeal and bacterial communities in subsurface marine sediments. Geomicrobiol J 27: 262-272.
14. Lin, Y.S., Lipp, J.S., Yoshinaga, M., Lin, S.H., Elvert, M., and Hinrichs, K.U. (2010b) Intramolecular stable carbon isotopic analysis of archaeal glycosyl tetraether lipids. Rapid Commun Mass Spectrom 24: 2817-2826.
15. Lipp, J.S., and Hinrichs, K.U. (2009) Structural diversity and fate of intact polar lipids in marine sediments. Geochim Cosmochim Acta 73: 6816-6833.
16. Lipp, J.S., Morono, Y., Inagaki, F., and Hinrichs, K.U. (2008) Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454: 991-994.
17. Liu, X., Leider, A., Gillespie, A., Gröger, J., Versteegh, G.J.M., and Hinrichs, K.U. (2010) Identification of polar lipid precursors of the ubiquitous branched GDGT orphan lipids in a peat bog in Northern Germany. Org Geochem 41: 653-660.
18. Liu, X., Lipp, J.S., Simpson, J.H., Lin, Y.S., Summons, R.E., and Hinrichs, K.U. (2012a) Mono- and dihydroxyl glycerol dibiphytanyl glycerol tetraethers in marine sediments: identification of both core and intact polar lipid forms. Geochim Cosmochim Acta 89: 102-115.
19. Liu, X., Lipp, J.S., Schröder, J.M., Summons, R.E., and Hinrichs, K.U. (2012b) Isoprenoidal glycerol dialkanol diethers: a series of novel archaeal lipids in marine sediments. Org Geochem 43: 50-55.
20. Logemann, J., Graue, J., Köster, J., Engelen, B., Rullkötter, J., and Cypionka, H. (2011) A laboratory experiment of intact polar lipid degradation in sandy sediments. Biogeosciences 8: 2547-2560.
21. Lomstein, B.A., Langerhuus, A.T., D'Hondt, S., Jørgensen, B.B., and Spivack, A.J. (2012) Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484: 101-104.
22. Morono, Y., Terada, T., Nishizawa, M., Ito, M., Hillion, F., Takahata, N., etal. (2011) Carbon and nitrogen assimilation in deep subseafloor microbial cells. Proc Natl Acad Sci USA 108: 18295-18300.
23. Parkes, R.J., Sellek, G., Webster, G., Martin, D., Anders, E., Weightman, A.J., and Sass, H. (2009) Culturable prokaryotic diversity of deep, gas hydrate sediments: first use of a continuous high-pressure, anaerobic, enrichment and isolation system for subseafloor sediments (DeepIsoBUG). Environ Microbiol 11: 3140-3153.
24. Pitcher, A., Hopmans, E.C., Mosier, A.C., Part, S.J., Rhee, S.K., Francis, C.A., etal. (2011) Core and intact polar glycerol dibiphytanyl glycerol tetraether lipids of ammonia-oxidizing archaea enriched from marine and estuarine sediments. Appl Environ Microbiol 77: 3468-3477.
25. Plasencia, A., Bañeras, L., Llirós, M., Casamayor, E.O., and Borrego, C. (2011) Maintenance of previously uncultured freshwater archaea from anoxic waters under laboratory conditions. Antonie Van Leeuwenhoek 99: 403-408.
26. Rossel, P.E., Lipp, J.S., Fredricks, H.F., Arnds, J., Boetius, A., Elvert, M., and Hinrichs, K.U. (2008) Intact polar lipids of anaerobic methanotrophic archaea and associated bacteria. Org Geochem 39: 992-999.
27. Rossel, P.E., Elvert, M., Rametter, A., Boetius, A., and Hinrichs, K.U. (2011) Factors controlling the distribution of anaerobic methanotrophic communities in marine environments: evidence from intact polar membrane lipids. Geochim Cosmochim Acta 75: 164-184.
28. Schippers, A., Neretin, L.N., Kallmeyer, J., Ferdelman, T.G., Cragg, B.A., Parkes, R.J., and Jørgensen, B.B. (2005) Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433: 861-864.
29. Schouten, S., Hopmans, E.C., Baas, M., Boumann, H., Standfest, S., Könneke, M., etal. (2008) Intact membrane lipids of 'Candidatus Nitrosopumilus maritimus', a cultivated representative of the cosmopolitan mesophilic Group I Crenarchaeota. Appl Environ Microbiol 74: 2433-2440.
30. Schouten, S., Middelburg, J.J., Hopmans, E.C., and Sinninghe Damsté, J.S. (2010) Fossilization and degradation of intact polar lipids in deep subsurface sediments: a theoretical approach. Geochim Cosmochim Acta 74: 3806-3814.
31. Schubotz, F., Wakeham, S.G., Lipp, J.S., Fredricks, H.F., and Hinrichs, K.U. (2009) Detection of microbial biomass by intact polar membrane lipid analysis in the water column and surface sediments of the Black Sea. Environ Microbiol 11: 2720-2734.
32. Schubotz, F., Lipp, J.S., Elvert, M., and Hinrichs, K.U. (2011) Stable carbon isotopic compositions of intact polar lipids reveal complex carbon flow patterns among hydrocarbon degrading microbial communities at the Chapopote asphalt volcano. Geochim Cosmochim Acta 75: 4399-4415.
33. Sinninghe Damsté, J.S., Schouten, S., Hopmans, E.C., van Duin, A.C.T., and Geenevasen, J.A.J. (2002) Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J Lipid Res 43: 1641-1651.
34. Sturt, H.F., Summons, R.E., Smith, K., Elvert, M., and Hinrichs, K.U. (2004) 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 18: 617-628.
35. Takano, Y., Chikaraishi, Y., Ogawa, N.O., Nomaki, H., Morono, Y., Inagaki, F., etal. (2010) Sedimentary membrane lipids recycled by deep-sea benthic archaea. Nat Geosci 3: 858-861.
36. Teske, A., and Sørensen, K.B. (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2: 3-18.
37. Tréhu, A.M., Bohrmann, G., Rack, F.R., Torres, M.E., etal. (2003) Proc ODP, Init Repts, 204. College Station, TX, USA: Ocean Drilling Program.
38. Wegener, G., Niemann, H., Elvert, M., Hinrichs, K.U., and Boetius, A. (2008) Assimilation of methane and inorganic carbon by microbial communities mediating the anaerobic oxidation of methane. Environ Microbiol 10: 2287-2298.
39. 13C-bicarbonate. Environ Microbiol 14: 1517-1527.
40. Whitman, W.B., Coleman, D.C., and Wiebe, W.J. (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95: 6578-6583.
41. Widdel, F., and Bak, F. (1992) Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes. Balows, A., Trüper, H.G., Dworkin, M., Harder, W., and Schleifer, K.H. (eds). New York, USA: Springer, pp. 3352-3378.