Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Chemosynthetic origin of 14C-depleted dissolved organic matter in a ridge-flank hydrothermal system

Abstract

Hydrothermal fluids circulate through extensive areas of the upper oceanic crust. Most hydrothermal circulation occurs on ridge flanks1,2, where low-temperature fluids flow through porous basalts. These fluids contain variable levels of dissolved organic carbon, but the source and composition of this carbon are uncertain. Here, we report Δ14C and δ13C measurements of dissolved organic carbon in ridge-flank and on-axis hydrothermal fluids sampled from the Juan de Fuca Ridge. Dissolved organic carbon from two independent ridge-flank sites was characterized by low δ13C and Δ14C values. The δ13C values ranged from −26 to −35, and were consistent with a chemoautotrophic origin. The 14C ages of the dissolved organic carbon ranged from 11,800 to 14,400 years before present, revealing that the carbon was around three times older than dissolved organics in the deep ocean. The Δ14C values of the ridge-flank dissolved organic matter also corresponded closely to those of dissolved inorganic carbon in the same fluid samples. Taken together, the data suggest that chemosynthetic crustal microbial communities synthesize dissolved organic carbon from inorganic carbon in ridge-flank fluids. We suggest that ridge-flank circulation may support an indigenous biosphere extensive enough to export substantial fixed carbon, with distinct isotopic and probably compositional character, to the overlying ocean.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Sampling locations on JDFR spreading centre.
Figure 2: Carbon isotopic composition of UDOC from low-temperature hydrothermal fluids.

Similar content being viewed by others

References

  1. Johnson, H. P. & Pruis, M. J. Fluxes of fluid and heat from the oceanic crustal reservoir. Earth Planet. Sci. Lett. 216, 565–574 (2003).

    Article  Google Scholar 

  2. Mottl, M. J. in Energy and Mass Transfer in Marine Hydrothermal Systems (eds Halbach, P. E., Tunnicliff, V. & Hein, J. R.) 271–286 (Dahlem Univ. Press, 2003).

    Google Scholar 

  3. Comita, P. B., Gagosian, R. B. & Williams, P. M. Suspended particulate organic material from hydrothermal vent waters at 21 N. Nature 307, 450–453 (1984).

    Article  Google Scholar 

  4. Hedges, J. I. Global biogeochemical cycles: Progress and problems. Mar. Chem. 39, 67–93 (1992).

    Article  Google Scholar 

  5. Druffel, E. R. M., Williams, P. M., Bauer, J. E. & Ertel, R. Cycling of dissolved and particulate organic matter in the open ocean. J. Geophys. Res. 97, 639–659 (1992).

    Article  Google Scholar 

  6. Lang, S. Q., Butterfield, D. A., Lilley, M. D., Paul Johnson, H. & Hedges, J. I. Dissolved organic carbon in ridge-axis and ridge-flank hydrothermal systems. Geochim. Cosmochim. Acta 70, 3830–3842 (2006).

    Article  Google Scholar 

  7. Walker, B., McCarthy, M. D., Fisher, A. & Guilderson, T. Dissolved inorganic carbon isotopic composition of low-temperature axial and ridge-flank hydrothermal fluids of the Juan de Fuca Ridge. Mar. Chem. 108, 123–136 (2008).

    Article  Google Scholar 

  8. Huber, J. A., Johnson, H. P., Butterfield, D. A. & Baross, J. A. Microbial life in ridge flank crustal fluids. Environ. Microbiol. 8, 88–99 (2006).

    Article  Google Scholar 

  9. Fisher, A. et al. Hydrothermal recharge and discharge across 50 km guided by seamounts on a young ridge flank. Nature 421, 618–620 (2003).

    Article  Google Scholar 

  10. Benner, R., Biddanda, B., Black, B. & McCarthy, M. Abundance, size distribution, and stable carbon and nitrogen isotope compositions of marine organic matter isolated by tangential-flow ultrafiltration. Mar. Chem. 57, 243–263 (1997).

    Article  Google Scholar 

  11. Proskurowskia, G., Lilley, M. D. & Brown, T. A. Isotopic evidence of magmatism and seawater bicarbonate removal at the endeavour hydrothermal system. Earth Planet. Sci. Lett. 225, 53–61 (2004).

    Article  Google Scholar 

  12. Taylor, G. T. et al. Chemoautotrophy in the redox transition zone of the Cariaco Basin: A significant midwater source of organic carbon production. Limnol. Oceanogr. 46, 148–163 (2001).

    Article  Google Scholar 

  13. Hayes, J. M., Strauss, H. & Kaufman, A. J. The abundance of C-13 in marine organic matter and isotopic fractionation in the global biogeochemical cycle of carbon during the past 800 Ma. Chem. Geol. 161, 103–125 (1999).

    Article  Google Scholar 

  14. House, C. H., Schopf, J. W. & Stetter, K. O. Carbon isotopic fractionation by Archaeans and other thermophilic prokaryotes. Org. Geochem. 34, 345–356 (2003).

    Article  Google Scholar 

  15. Cowen, J. P. et al. Fluids from aging ocean crust that support microbial life. Science 299, 120–123 (2003).

    Article  Google Scholar 

  16. Williams, P. M. & Druffel, E. R. M. Radiocarbon in dissolved organic matter in the central North Pacific Ocean. Nature 330, 246–248 (1987).

    Article  Google Scholar 

  17. Loh, A. I., Bauer, J. E. & Druffel, E. R. M. Variable ageing and storage of dissolved organic components in the open ocean. Nature 430, 877–881 (2004).

    Article  Google Scholar 

  18. Guo, L., Santschi, P. H., Cifuentes, L. A., Trumbore, S. E. & Southon, J. Cycling of high-molecular-weight dissolved organic matter in the Middle Atlantic Bight as revealed by carbon isotopic (13C and 14C) signatures. Limnol. Oceanogr. 41, 1242–1252 (1996).

    Article  Google Scholar 

  19. Hernes, P. J. & Benner, R. Transport and diagenesis of dissolved and particulate terrigenous organic matter in the North Pacific Ocean. Deep-Sea Res. I 49, 2119–2132 (2002).

    Article  Google Scholar 

  20. Lilley, M. D. et al. Anomalous CH4 and NH4+ concentrations at an unsedimented mid-ocean-ridge hydrothermal system. Nature 364, 45–47 (1993).

    Article  Google Scholar 

  21. Johnson, H. P. et al. Probing for life in the ocean crust with the LEXEN program. EOS 84, 109–116 (2003).

    Article  Google Scholar 

  22. Keil, R. G., Tsamakis, E., Fuh, C. B., Giddings, J. C. & Hedges, J. I. Mineralogical and textural controls on the organic composition of coastal marine sediments: hydrodynamic separation using SPLITT-fractionation. Geochim. Cosmochim. Acta 58, 879–893 (1994).

    Article  Google Scholar 

  23. Heuer, V. B., Pohlman, J. W., Torres, M. E., Elvert, M. & Hinrichs, K. U. The stable carbon isotope biogeochemistry of acetate and other dissolved carbon species in deep subseafloor sediments at the northern Cascadia Margin. Geochim. Cosmochim. Acta 73, 3323–3336 (2009).

    Article  Google Scholar 

  24. Lang, S. Q., Butterfield, D. A., Schulte, M., Kelley, D. S. & Lilley, M. D. Elevated concentrations of formate, acetate and dissolved organic carbon found at the Lost City hydrothermal field. Geochim. Cosmochim. Acta 74, 941–952 (2010).

    Article  Google Scholar 

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

    Article  Google Scholar 

  26. McCollom, T. M. & Seewald, J. S. Abiotic synthesis of organic compounds in deep-sea hydrothermal environments. Chem. Rev. 107, 382–401 (2007).

    Article  Google Scholar 

  27. Hernes, P. J. & Benner, R. Photochemical and microbial degradation of dissolved lignin phenols: Implications for the fate of terrigenous dissolved organic matter in marine environments. J. Geophys. Res. 108, 3291 (2003).

    Article  Google Scholar 

  28. Santelli, C. M. et al. Abundance and diversity of microbial life in ocean crust. Nature 453, 653–656 (2008).

    Article  Google Scholar 

  29. Bach, W. & Edwards, K. J. Iron and sulfide oxidation within the basaltic ocean crust: Implications for chemolithoautotrophic microbial biomass production. Geochim. Cosmochim. Acta 67, 3871–3887 (2003).

    Article  Google Scholar 

  30. Beaupré, S. R., Druffel, E. R. M. & Griffin, S. A low-blank photochemical extraction system for concentration and isotopic analyses of marine dissolved organic carbon. Limnol. Oceanogr. Methods 5, 174–184 (2007).

    Article  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the assistance at sea of our co-investigators on the LEXEN project, especially H. Paul Johnson, S. Lang and T. Bjorklund. We also thank A. Fisher and D. Butterfield for comments and insight regarding the JDFR system, and D. Butterfield for sharing inorganic composition data. This work was supported by NSF (LEXEN programme), as well as grants from the University of California Office of the President (CLC programme) and the Packard Foundation.

Author information

Authors and Affiliations

Authors

Contributions

M.D.M. planned the project, supervised sampling and analyses, analysed data and wrote the paper; B.D.W. designed and carried out UDOC isolations and sample processing, analysed and plotted data. I.V. designed sampling and ultrafiltration equipment, carried out UDOC isolations and assisted with sample processing. S.R.B. carried out 14C-UDOC sample analyses and analysed data. T.P.G. and E.R.M.D. supervised 14C sample analyses and interpreted data.

Corresponding author

Correspondence to Matthew D. McCarthy.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 428 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

McCarthy, M., Beaupré, S., Walker, B. et al. Chemosynthetic origin of 14C-depleted dissolved organic matter in a ridge-flank hydrothermal system. Nature Geosci 4, 32–36 (2011). https://doi.org/10.1038/ngeo1015

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo1015

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology