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Significant contribution of Archaea to extant biomass in marine subsurface sediments

Nature volume 454, pages 991994 (21 August 2008) | Download Citation

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Abstract

Deep drilling into the marine sea floor has uncovered a vast sedimentary ecosystem of microbial cells1,2. Extrapolation of direct counts of stained microbial cells to the total volume of habitable marine subsurface sediments suggests that between 56 Pg (ref. 1) and 303 Pg (ref. 3) of cellular carbon could be stored in this largely unexplored habitat. From recent studies using various culture-independent techniques, no clear picture has yet emerged as to whether Archaea or Bacteria are more abundant in this extensive ecosystem4,5,6,7. Here we show that in subsurface sediments buried deeper than 1 m in a wide range of oceanographic settings at least 87% of intact polar membrane lipids, biomarkers for the presence of live cells7,8, are attributable to archaeal membranes, suggesting that Archaea constitute a major fraction of the biomass. Results obtained from modified quantitative polymerase chain reaction and slot-blot hybridization protocols support the lipid-based evidence and indicate that these techniques have previously underestimated archaeal biomass. The lipid concentrations are proportional to those of total organic carbon. On the basis of this relationship, we derived an independent estimate of amounts of cellular carbon in the global marine subsurface biosphere. Our estimate of 90 Pg of cellular carbon is consistent, within an order of magnitude, with previous estimates, and underscores the importance of marine subsurface habitats for global biomass budgets.

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References

  1. 1.

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

  2. 2.

    et al. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216–2221 (2004)

  3. 3.

    , & Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998)

  4. 4.

    et al. Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861–864 (2005)

  5. 5.

    et al. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc. Natl Acad. Sci. USA 103, 2815–2820 (2006)

  6. 6.

    , , & Direct in situ detection of cells in deep-sea sediment cores from the Peru Margin (ODP Leg 201, Site 1229). Geobiology 2, 217–223 (2004)

  7. 7.

    et al. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc. Natl Acad. Sci. USA 103, 3846–3851 (2006)

  8. 8.

    , , , & 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. Rap. Comm. Mass. Spec. 18, 617–628 (2004)

  9. 9.

    et al. Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl. Environ. Microbiol. 69, 7224–7235 (2003)

  10. 10.

    et al. Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436, 390–394 (2005)

  11. 11.

    , , , & in Methodology for Biomass Determination and Microbial Activities in Sediments (eds Lichtfeld, C. D. & Seyfried, P. L.) 87–103 (ASTM STP 673, 1979)

  12. 12.

    , , & Phospholipid analysis as a tool to study complex microbial communities in marine sediments. J. Microbiol. Methods 48, 149–160 (2002)

  13. 13.

    , , , & Intact phospholipids—microbial ‘‘life markers’’ in marine deep subsurface sediments. Org. Geochem. 34, 755–769 (2003)

  14. 14.

    & Data report: intact membrane lipids as indicators of subsurface life in Cretaceous and Paleogene sediments from Sites 1257 and 1258. Proc. ODP Sci. Res. 207 10.2973/odp.proc.sr.207.112.2007 (2007)

  15. 15.

    & Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol. Prog. Ser. 51, 201–213 (1989)

  16. 16.

    Microbial communities of deep marine subsurface sediments: molecular and cultivation surveys. Geomicrobiol. J. 23, 357–368 (2006)

  17. 17.

    , , , & Phospholipid fatty acid-derived microbial biomass and community dynamics in hot, hydrothermally influenced sediments from the Middle Valley, Juan de Fuca Ridge. Proc. ODP Sci. Res. 169 10.2973/odp.proc.sr.169.117.2000 (2000)

  18. 18.

    , , & Habitability of subseafloor sediments at the Costa Rica Convergent Margin. Proc. ODP Sci. Res. 205 10.2973/odp.proc.sr.205.213.2006 (2006)

  19. 19.

    , , , & Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc. Natl Acad. Sci. USA 103, 8607–8612 (2006)

  20. 20.

    & Organic carbon degradation in arctic marine sediments, Svalbard: A comparison of initial and terminal steps. Geomicrobiol. J. 23, 551–563 (2006)

  21. 21.

    et al. Biomarkers at the microscopic range: ToF-SIMS molecular imaging of Archaea-derived lipids in a microbial mat. Geobiology 5, 413–421 (2007)

  22. 22.

    , & Recent studies on bacterial populations and processes in subseafloor sediments: a review. Hydrogeol. J. 8, 11–28 (2000)

  23. 23.

    & Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J. 2, 3–18 (2008)

  24. 24.

    , , & Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bact. 186, 2629–2635 (2004)

  25. 25.

    Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nature Rev. Microbiol. 5, 316–323 (2007)

  26. 26.

    , , & Organic carbon content in surface sediments—defining regional provinces. Deep-Sea Res. I 51, 2001–2026 (2004)

  27. 27.

    , & Organic matter mineralization in marine systems. Glob. Plan. Change 8, 47–58 (1993)

  28. 28.

    & The carbon cycle and associated redox processes through time. Phil. Trans. R. Soc. B. 361, 931–950 (2006)

  29. 29.

    & Glacial/interglacial variations in atmospheric carbon dioxide. Nature 407, 859–869 (2000)

  30. 30.

    , & Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001)

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Acknowledgements

Samples for this research were provided by the Integrated Ocean Drilling Program (IODP, expeditions 301 and 311), the Ocean Drilling Program (ODP, legs 201, 204 and 207; sponsored by the US National Science Foundation and participating countries under the Joint Oceanographic Institutions, Inc.), and cruises Sonne SO147, Kaiyo KY04-11, Professor Logatchev TTR15 and Chikyu Shakedown Expedition CK06-06. We thank the participating crews and scientists for sample recovery and data; U. Proske and N. Buchs for assistance with lipid extraction and sample preparation; J. M. Hayes and A. Teske for comments on an earlier version of this manuscript; H. F. Fredricks and F. Schubotz for discussion of data; V. Heuer, A. Schippers and T. Toki for sample donation; B. Kockisch for TOC analysis; and T. Terada and N. Masui for DNA extraction and analyses. This work was supported by Deutsche Forschungsgemeinschaft (through MARUM Center for Marine Environmental Sciences and grant Hi616-4 from the priority program IODP/ODP) and JAMSTEC Multidisciplinary Research Promotion Award 2007 (to Y.M. and F.I.). This is MARUM publication number 0585.

Author Contributions J.S.L., geochemical and lipid analysis, geochemical modelling, method development and paper writing; Y.M. and F.I., DNA extraction and molecular analyses; K.-U.H., study design, paper writing and geochemical modelling. All authors participated in data analysis and interpretation and provided editorial comments on the manuscript.

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Affiliations

  1. Organic Geochemistry Group, Department of Geosciences and MARUM Center for Marine Environmental Sciences, University of Bremen, PO Box 330 440, 28334 Bremen, Germany

    • Julius S. Lipp
    •  & Kai-Uwe Hinrichs
  2. Geomicrobiology Group, Kochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Monobe B200, Nankoku, Kochi 783-8502, Japan

    • Yuki Morono
    •  & Fumio Inagaki

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Correspondence to Kai-Uwe Hinrichs.

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    Supplementary Information 1

    This file contains Supplementary Methods, Supplementary Figures 1-4, Supplementary Tables 1-5, and additional references.

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https://doi.org/10.1038/nature07174

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