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Methane-consuming archaebacteria in marine sediments

Abstract

Large amounts of methane are produced in marine sediments but are then consumed before contacting aerobic waters or the atmosphere1. Although no organism that can consume methane anaerobically has ever been isolated, biogeochemical evidence indicates that the overall process involves a transfer of electrons from methane to sulphate and is probably mediated by several organisms, including a methanogen (operating in reverse) and a sulphate-reducer (using an unknown intermediate substrate)2. Here we describe studies of sediments related to a decomposing methane hydrate. These provide strong evidence that methane is being consumed by archaebacteria that are phylogenetically distinct from known methanogens. Specifically, lipid biomarkers that are commonly characteristic of archaea are so strongly depleted in carbon-13 that methane must be the carbon source, rather than the metabolic product, for the organisms that have produced them. Parallel gene surveys of small-subunit ribosomal RNA (16S rRNA) indicate the predominance of a new archael group which is peripherally related to the methanogenic orders Methanomicrobiales and Methanosarcinales.

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Figure 1: Reconstructed-ion-current chromatograms of trimethylsilylated total lipid extracts from a, a sample 13–15?cm below the sediment surface at a site of active methane seepage (PC26, Eel River Basin) and b, a control sample 33–36?cm below the sediment surface in the same basin but remote from any site of methane release (HPC 5).
Figure 2: Electron-impact mass spectrum of peak 2, Fig. 1a.
Figure 3: Phylogenetic analysis of archaeal ribosomal rRNA sequences recovered from seep sediments in the Eel River Basin.

References

  1. 1

    Reeburgh, W. S. in Microbial Growth on C1 Compounds (eds. Lidstrom, M. E. & Tabita, F. R.) 334–342 (Kluwer Academic Publishers, Dordrecht, (1996).

    Book  Google Scholar 

  2. 2

    Hoehler, T. M. & Alperin, M. J. in Microbial Growth on C1 Compounds (eds. Lidstrom, M. E. & Tabita, F. R.) 326–333 (Kluwer Academic Publishers, Dordrecht, (1996).

    Book  Google Scholar 

  3. 3

    Brooks, J. M., Field, M. E. & Kennicutt, M. C. II. Observations of gas hydrates in marine sediments, offshore Northern California. Mar. Geol. 96, 103–109 (1991).

    ADS  CAS  Article  Google Scholar 

  4. 4

    Hayes, J. M., Freeman, K. H., Popp, B. N. & Hoham, C. H. Compound-specific isotopic analyses: A novel tool for reconstruction of ancient biogeochemical processes. Org. Geochem. 16, 1115–1128 (1990).

    CAS  Article  Google Scholar 

  5. 5

    Pace, N. R. Amolecular view of microbial diversity and the biosphere. Science 276, 734–740 (1997).

    CAS  Article  Google Scholar 

  6. 6

    Tornabene, T. G. & Langworthy, T. G. Diphytanyl and dibiphytanyl glycerol ether lipids of methanogenic Archaebacteria. Science 203, 51–53 (1979).

    ADS  CAS  Article  Google Scholar 

  7. 7

    Teixidor, P. & Grimalt, J. O. Gas chromatographic determination of isoprenoid alkylglycerol diethers in archaebacterial cultures and environmental samples. J. Chromatogr. 607, 253–259 (1992).

    CAS  Article  Google Scholar 

  8. 8

    Koga, Y., Morii, H., Akagawa-Matsushita, M. & Ohga, M. Correlation of polar lipid composition with 16S rRNA phylogeny in methanogens. Further analysis of lipid component parts. Biosci. Biotechnol. Biochem. 62, 230–236 (1998).

    CAS  Article  Google Scholar 

  9. 9

    Belyaev, S. S.et al. Methanogenic bacteria from the Bondyuzhskoe Oil Field: general characterization and analysis of stable-carbon isotopic fractionation. Appl. Env. Microbiol. 45, 691–697 (1983).

    CAS  Google Scholar 

  10. 10

    Irwin, H., Curtis, C. & Coleman, M. Isotopic evidence for source of diagenetic carbonates formed during burial of organic-rich sediments. Nature 269, 209–213 (1977).

    ADS  CAS  Article  Google Scholar 

  11. 11

    Freeman, K. H., Hayes, J. M., Trendel, J.-M. & Albrecht, P. Evidence from carbon isotope measurements for diverse origins of sedimentary hydrocarbons. Nature 343, 254–256 (1990).

    ADS  CAS  Article  Google Scholar 

  12. 12

    Summons, R. E., Jahnke, L. L. & Roksandic, Z. Carbon isotopic fractionation in lipids from methanotrophic bacteria: Relevance for interpretation of the geochemical record of biomarkers. Geochim. Cosmochim. Acta 58, 2853–2863 (1994).

    ADS  CAS  Article  Google Scholar 

  13. 13

    Boone, D. R., Whitman, W. B. & Rouvière, P. in Methanogens: Ecology, Physiology, Biochemistry, and Genetics (ed. Ferry J. J.) 35–80 (Chatman & Hall, New York and London, (1993).

  14. 14

    Munson, M. A., Nedwell, D. B. & Embley, T. M. Phylogenetic diversity of Archaea in sediment samples from a coastal salt marsh. Appl. Environ. Microbiol. 63, 4729–4733 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Hershberger, K. L., Barns, S. M., Reysenbach, A. L., Dawson, S. C. & Pace, N. R. Crenarchaeota in low-temperature terrestrial environments. Nature 384, 420 (1996).

    ADS  CAS  Article  Google Scholar 

  16. 16

    Kato, C., Li, L., Tamaoka, J. & Horikoshi, K. Molecular analyses of the sediment of the 11000m deep Mariana Trench. Extremophiles 1, 117–123 (1997).

    CAS  Article  Google Scholar 

  17. 17

    McGregor, B. J., Moser, D. P., Alm, E. W., Nealson, K. H. & Stahl, D. A. Crenarchaeota in Lake Michigan sediment. Appl. Environ. Microbiol. 63, 1178–1181 (1997).

    Google Scholar 

  18. 18

    Vetriani, C., Reysenbach, A. L. & Doré, J. Recovery and phylogenetic analysis of archaeal rRNA sequences from continental shelf sediments. FEMS Microbiol. Lett. 161, 83–88 (1998).

    CAS  Article  Google Scholar 

  19. 19

    Großkopf, R., Stubner, S. & Liesack, W. Novel euryarchaeal lineages detected on rice roots and in anoxic bulk soil of flooded rice microcosms. Appl. Environ. Microbiol. 64, 4983–4989 (1998).

    PubMed Central  Google Scholar 

  20. 20

    Sprott, G. D., Dicaire, C. J., Choquet, C. G., Patel, G. B. & Ekeil, I. Hydroxydiether lipid structures in Methanosarcina spp. and Methanococcus voltae. Appl. Environ. Microbiol. 59, 912–914 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21

    Zehnder, A. J. B. & Brock, T. D. Methane formation and methane oxidation by methanogenic bacteria. J. Bacteriol. 137, 420–432 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Harder, J. Anaerobic methane oxidation by bacteria employing 14C-methane uncontaminated with 14C-carbon monoxide. Mar. Geol. 137, 13–23 (1997).

    ADS  CAS  Article  Google Scholar 

  23. 23

    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. Glob. Biogeochem. Cycles 8, 451–463 (1994).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Hansen, L. B., Finster, K., Fossing, H. & Iversen, N. Anaerobic methane oxidation in sulfate depleted sediments: effects of sulfate and molybdate additions. Aquat. Microb. Ecol. 14, 195–204 (1998).

    Article  Google Scholar 

  25. 25

    Summons, R. E., Franzmann, P. D. & Nichols, P. D. Carbon isotopic fractionation associated with methylotrophic methanogenesis. Org. Geochem. 28, 465–476 (1998).

    CAS  Article  Google Scholar 

  26. 26

    Bian, L. Isotopic Biogeochemistry of Individual Compounds in a Modern Coastal Marine Sediment (Kattegat, Denmark and Sweden). Thesis, Indiana Univ.(1994).

  27. 27

    Holzer, G., Oro, J. & Tornabene, T. G. Gas chromatographic-mass spectrometric analysis of neutral lipids from methanogenic and thermacidophilic bacteria. J. Chromatogr. 18, 795–809 (1979).

    Article  Google Scholar 

  28. 28

    Kvenvolden, K. A. in Gas Hydrates: Relevance ot the World Margin Stability and Climate Change (eds Henriet, J. P. & Mienert, J.) 9–30 (Geological Society, London, (1998).

  29. 29

    DeLong, E. F. Archaea in coastal marine environments. Proc. Natl Acad. Sci. USA 89, 5685–5689 (1992).

    ADS  CAS  Article  Google Scholar 

  30. 30

    Massana, R., Murray, A. E., Preston, C. M. & DeLong, E. F. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl. Environ. Microbiol. 63, 50–56 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank C. Johnson and L. Houghton for isotopic analyses; D. Orange and K.Kvenvolden for collecting some of the sediment samples; P. D. Nichols and R. Summons for an extract of M. burtonii; A. Teske, J. Rullkötter, R. E. Summons, and T. Hoehler for discussions; and the officers and crew of the Pt. Lobos, and pilots of the ROV Ventana, for expert assistance. K.H. is supported by a research fellowship from the Deutsche Forschungsgemeinschaft. J.M.H., S.P.S., and laboratory expenses were supported by NASA. The Eel River expedition and E.F.D. and P.G.B. supported by the David and Lucile Packard Foundation.

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Correspondence to John M. Hayes.

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Hinrichs, KU., Hayes, J., Sylva, S. et al. Methane-consuming archaebacteria in marine sediments. Nature 398, 802–805 (1999). https://doi.org/10.1038/19751

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