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Significant contribution of Archaea to extant biomass in marine subsurface sediments


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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Figure 1: Depth profiles of IPLs in marine sediments.
Figure 2: Relative abundance of archaeal 16S rRNA genes to total archaeal and bacterial 16S rRNA genes.
Figure 3: Correlation of concentrations of IPLs and TOC.


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

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  3. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  5. Inagaki, F. 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)

    Article  ADS  CAS  Google Scholar 

  6. Mauclaire, L., Zepp, K., Meister, P. & McKenzie, J. 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)

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. Sturt, H. F., Summons, R. E., Smith, K. J., 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. Rap. Comm. Mass. Spec. 18, 617–628 (2004)

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  11. White, D. C., Bobbie, R. J., King, J. D., Nickels, J. S. & Amoe, P. in Methodology for Biomass Determination and Microbial Activities in Sediments (eds Lichtfeld, C. D. & Seyfried, P. L.) 87–103 (ASTM STP 673, 1979)

    Book  Google Scholar 

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

    Article  Google Scholar 

  13. Zink, K. G., Wilkes, H., Disko, U., Elvert, M. & Horsfield, B. Intact phospholipids—microbial ‘‘life markers’’ in marine deep subsurface sediments. Org. Geochem. 34, 755–769 (2003)

    Article  CAS  Google Scholar 

  14. Fredricks, H. F. & Hinrichs, K.-U. 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/ (2007)

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

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Summit, M., Peacock, A., Ringelberg, D., White, D. C. & Baross, J. A. 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/ (2000)

  18. Cardace, D., Morris, J. D., Peacock, A. D. & White, D. C. Habitability of subseafloor sediments at the Costa Rica Convergent Margin. Proc. ODP Sci. Res. 205 10.2973/ (2006)

  19. Van Mooy, B. A. S., Rocap, G., Fredricks, H. F., Evans, C. T. & Devol, A. H. Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc. Natl Acad. Sci. USA 103, 8607–8612 (2006)

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Parkes, R. J., Cragg, B. A. & Wellsbury, P. Recent studies on bacterial populations and processes in subseafloor sediments: a review. Hydrogeol. J. 8, 11–28 (2000)

    Article  ADS  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Acinas, S. G., Marcelino, L., Klepac-Ceraj, V. & Polz, M. F. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bact. 186, 2629–2635 (2004)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  26. Seiter, K., Hensen, C., Schröter, J. & Zabel, M. Organic carbon content in surface sediments—defining regional provinces. Deep-Sea Res. I 51, 2001–2026 (2004)

    Article  CAS  Google Scholar 

  27. Middelburg, J. J., Vlug, T. & van der Nat, F. J. W. A. Organic matter mineralization in marine systems. Glob. Plan. Change 8, 47–58 (1993)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Sigman, D. M. & Boyle, E. A. Glacial/interglacial variations in atmospheric carbon dioxide. Nature 407, 859–869 (2000)

    Article  ADS  CAS  Google Scholar 

  30. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001)

    Article  ADS  CAS  Google Scholar 

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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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Correspondence to Kai-Uwe Hinrichs.

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Lipp, J., Morono, Y., Inagaki, F. et al. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454, 991–994 (2008).

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