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Deep marine biosphere fuelled by increasing organic matter availability during burial and heating

Nature volume 388, pages 573–576 (1997)Cite this article

Abstract

Deep-sea sediments become apparently more hostile to life with increasing depth as temperature and pressure rise, and organic matter becomes increasingly recalcitrant. Demonstrations of high bacterial populations in deep sediments1,2 may thus appear enigmatic. How, then, can the continued presence of active bacterial populations in deep sediments that are over 10 million years old be explained? Although volatile fatty acids, particularly acetate, are important intermediates in the anaerobic degradation of organic matter3,4, their concentrations are kept very low in sediments (<15 µM) by rapid bacterial consumption5,6. Here we show that heating surface coastal marine sediments to simulate increasing temperature during burial produces an increase of over three orders of magnitude in acetate concentration and increases bacterial activity. We found that pore-water acetate concentration at two sites in the Atlantic Ocean increased at depths below about 150 m and was associated with a significant stimulation in bacterial activity. Comparing these acetate concentrations to in situ temperatures confirmed that there was a notable generation of acetate associated with temperature increases during burial. This was supported by heating experiments with deep sediments. Thus, acetate generation from organic matter during burial may explain the presence of a deep bacterial biosphere in marine sediments, and could underpin an even deeper and hotter biosphere than has previously been considered.

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Figure 1: Generation of pore-water acetate from a coastal near-surface sediment exposed to low-temperature heating.
Figure 2: Depth profiles of pore-water acetate concentrations and rates of bacterial activity in sediments from Blake Ridge, ODP Leg 164, Site 995.
Figure 3: Comparison of in situ pore-water acetate concentrations from Blake Ridge sediments with experimental low-temperature acetate generation from near-surface coastal sediments.
Figure 4: Generation of acetate from deep-sediment samples subjected to low-temperature heating.

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References

  1. Parkes, R. J.et al. Deep bacterial biosphere in Pacific Ocean sediments. Nature 371, 410–413 (1994).

    Article  ADS  Google Scholar 

  2. Cragg, B. A.et al. Bacterial populations and processes in sediments containing gas hydrates (ODP Leg 146: Cascadia Margin). Earth Planet. Sci. Lett. 139, 497–507 (1996).

    Article  ADS  CAS  Google Scholar 

  3. Sørensen, J., Christensen, D. & Jørgensen, B. B. Volatile fatty acids and hydrogen as substrates for sulfate-reducing bacteria in anaerobic marine sediment. Appl. Environ. Microbiol. 42, 5–11 (1981).

    PubMed  PubMed Central  Google Scholar 

  4. Winfrey, M. R. & Ward, D. M. Substrates for sulfate reduction and methane production in intertidal sediments. Appl. Environ. Microbiol. 45, 193–199 (1983).]

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Jørgensen, B. B. Mineralisation of organic matter in the sea bed: The role of sulphate reduction. Nature 296, 643–645 (1982).

    Article  ADS  Google Scholar 

  6. Wellsbury, P. & Parkes, R. J. Acetate bioavailability and turnover in an estuarine sediment. FEMS Microbiol. Ecol. 17, 85–94 (1995).

    Article  CAS  Google Scholar 

  7. Whiticar, M. J., Faber, E. & Schoell, M. Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation: Isotope evidence. Geochim. Cosmochim. Acta 50, 693–709 (1986).

    Article  ADS  CAS  Google Scholar 

  8. Cooles, G. P., Mackenzie, A. S. & Parkes, R. J. Non-hydrocarbons of significance in petroleum exploration: Volatile fatty acids and non-hydrocarbon gases. Mineral. Mag. 51, 483–493 (1987).

    Article  CAS  Google Scholar 

  9. Borgund, A. E. & Barth, T. Generation of short-chain organic-acids from crude-oil by hydrous pyrolysis. Org. Geochem. 21, 943–952 (1994).

    Article  CAS  Google Scholar 

  10. Whelan, J. K.et al. Evidence for sulfate-reducing and methane-producing organisms in sediments from Sites 618, 619 and 622. Init. Rep. Deep-Sea Drill. Proj. 96, 767–775 (1986).

    CAS  Google Scholar 

  11. King, G. M. Measurement of acetate concentrations in marine pore water by using an enzymatic approach. Appl. Environ. Microbiol. 57, 3476–3481 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Dickens, G. R.et al. Direct measurements of in situ methane quantities in a large gas-hydrate reservoir. Nature 385, 426–428 (1997).

    Article  ADS  CAS  Google Scholar 

  13. Cragg, B. A.et al. Bacterial biomass and activity profiles within deep sediment layers. Proc. ODP Sci. Res. 112, 607–619 (1990).

    CAS  Google Scholar 

  14. Wellsbury, P., Herbert, R. A. & Parkes, R. J. Bacterial activity and production in near-surface estuarine and freshwater sediments. FEMS Microbiol. Ecol. 19, 203–214 (1996).

    Article  CAS  Google Scholar 

  15. Paull, C. K.et al. Leg 164—gas hydrate sampling on the Blake Ridge and Carolina Rise. Proc. ODP Init. Rep. 164, 623 ((1966)).

    Google Scholar 

  16. Barth, T. Quantitative determination of volatile carboxylic acids in formation water by isotachophoresis. Anal. Chem. 59, 2232–2237 (1987).

    Article  CAS  Google Scholar 

  17. Stetter, K. O. Hyperthermophiles in the history of life. Ciba Found. Symp. 202, 1–18 (1996).

    CAS  PubMed  Google Scholar 

  18. Cragg, B. A. & Parkes, R. J. Bacterial profiles in hydrothermally active deep sediment layers from Middle Valley (N.E. Pacific) Sites 857 and 858. Proc. ODP Sci. Res. 139, 509–516 (1993).

    Google Scholar 

  19. Haridon, S. L., Reysenbach, A., Glenat, P., Prieur, D. & Jeanthon, C. Hot subterranean biosphere in continental oil reservoir. Nature 377, 223–224 (1995).

    Article  ADS  Google Scholar 

  20. Galimov, E. M. & Kvenvolden, K. A. Concentrations and carbon isotopic compositions of CH4 and CO2 in gas from sediments of the Blake Outer Ridge, Deep-Sea Drilling Project Leg 76. Init. Rep. Deep-Sea Drill. Proj. 76, 403–407 (1983).

    CAS  Google Scholar 

  21. de Graaf, W., Wellsbury, P., Parkes, R. J. & Cappenberg, T. E. Comparison of acetate turnover in methanogenic and sulfate-reducing sediments by radio- and stable-isotope-labeling and specific inhibitors: Evidence for isotopic exchange. Appl. Environ. Microbiol. 62, 772–777 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Cragg, B. A.et al. Bacterial profiles in deep sediments of the Santa Barbara Basin Site 893. Proc. ODP Sci. Res. 146, 139–144 (1995).

    Google Scholar 

  23. Cragg, B. A.et al. The impact of fluid and gas venting on bacterial populations and processes in sediments from the Cascadia Margin accretionary system (sites 888–892) and the geochemical consequences. Proc. ODP Sci. Res. 146, 399–411 (1995).

    CAS  Google Scholar 

  24. Furnes, H., Thorseth, I. H., Tumyr, O., Torsvik, T. & Fisk, M. R. Microbial activity in the alteration of glass from pillow lavas from Hole 896A. Proc. ODP Sci. Res. 148, 191–214 (1996).

    Google Scholar 

  25. Giovannoni, S. J., Fisk, M. R., Mullins, T. D. & Furnes, H. Genetic evidence for endolithic microbial life colonising basaltic glass/seawater interfaces. Proc. ODP Sci. Res. 148, 207–214 (1996).

    Google Scholar 

  26. Rochelle, P. A., Fry, J. C., Parkes, R. J. & Weightman, A. J. DNA extraction for 16S rRNA gene analysis for determining genetic diversity in deep sediment communities. FEMS Microbiol. Lett. 100, 59–66 (1992).

    Article  CAS  PubMed  Google Scholar 

  27. Parkes, R. J.et al. Biogeochemical processes in gas hydrate zones. Abstracts, Exploration and exploitation of non-living deep-sea marine resources.Challenger Society for Marine Science & Geological Society, Marine Studies Group(Geological Society, London, (1996)).

  28. Jørgensen, B. B., Isaksen, M. F. & Jannasch, H. W. Bacterial sulfate reduction above 100 °C in deep-sea hydrothermal sediments. Science 258, 1756–1757 (1992).

    Article  ADS  PubMed  Google Scholar 

  29. Parkes, R. J. & Taylor, J. Analysis of volatile fatty acids by ion-exclusion chromatography, with special reference to marine pore water. Mar. Biol. 77, 113–118 (1983).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank ODP for allowing us to obtain samples on Leg 164; T. Woodward and I. Mather for their assistance with sample collection and initial handling in the laboratory; J. Maxwell, E. Shock and J. Whelan for comments on the original manuscript; P. Egeberg for facilitating analysis of Site 997; M. Isaksen for details of the thermal gradient system, and F. Wheeler for its construction. This work was funded by the European Union Environment Programme and the Natural Environment Research Council (UK).

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Authors and Affiliations

  1. Department of Geology, University of Bristol, Wills Memorial Building, Queens Road, BS8 1RJ, Bristol, UK

    Peter Wellsbury, Kim Goodman, Barry A. Cragg, Stephen P. Barnes & R. John Parkes

  2. Department of Chemistry, University of Bergen, Allegt, 41, N-5007, Bergen, Norway

    Tanja Barth

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Correspondence to R. John Parkes.

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Wellsbury, P., Goodman, K., Barth, T. et al. Deep marine biosphere fuelled by increasing organic matter availability during burial and heating. Nature 388, 573–576 (1997). https://doi.org/10.1038/41544

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