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:

The Santa Barbara Basin is a symbiosis oasis

Abstract

It is generally agreed that the origin and initial diversification of Eucarya occurred in the late Archaean or Proterozoic Eons when atmospheric oxygen levels were low1 and the risk of DNA damage due to ultraviolet radiation was high2. Because deep water provides refuge against ultraviolet radiation3 and early eukaryotes may have been aerotolerant anaerobes1,4,5, deep-water dysoxic environments are likely settings for primeval eukaryotic diversification. Fossil evidence shows that deep-sea microbial mats, possibly of sulphur bacteria similar to Beggiatoa, existed during that time6. Here we report on the eukaryotic community of a modern analogue, the Santa Barbara Basin (California, USA). The Beggiatoa mats of these severely dysoxic and sulphidic sediments support a surprisingly abundant protistan and metazoan meiofaunal community, most members of which harbour prokaryotic symbionts. Many of these taxa are new to science, and both microaerophilic and anaerobic taxa appear to be represented. Compared with nearby aerated sites, the Santa Barbara Basin is a ‘symbiosis oasis’ offering a new source of organisms for testing symbiosis hypotheses of eukaryogenesis.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Abundance and biovolume of SBB meiofauna.
Figure 2: Micrographs of SBB meiofauna with symbionts.

Similar content being viewed by others

References

  1. Knoll,A. H. & Holland,H. D. in Effects of Past Global Change on Life 21–33 (National Research Council, Washington, DC, 1995).

    Google Scholar 

  2. Kasting,J. F. Earth's early atmosphere. Science 259, 920–926 (1993).

    Article  ADS  CAS  Google Scholar 

  3. Cockell,C. S. Biological effects of high ultraviolet radiation on early Earth—a theoretical evaluation. J. Theor. Biol. 193, 717–729 (1998).

    Article  CAS  Google Scholar 

  4. Martin,W. & Müller,M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).

    Article  ADS  CAS  Google Scholar 

  5. Moreira,D. & López-García,P. Symbiosis between methanogenic Archaea and δ-Proteobacteria as the origin of eukaryotes: The syntrophic hypothesis. J. Mol. Evol. 47, 517–530 (1998).

    Article  ADS  CAS  Google Scholar 

  6. Simonson,B. M. & Carney,K. E. Roll-up structures: evidence of in situ microbial mats in Late Archaean deep shelf environments. Palaios 14, 13–24 (1999).

    Article  ADS  Google Scholar 

  7. Reimers,C. E. et al. Porewater pH and authigenic phases formed in the uppermost sediments of the Santa Barbara Basin. Geochim. Cosmochim. Acta 60, 4037–4057 (1996).

    Article  ADS  CAS  Google Scholar 

  8. Kuwabara,J. S. et al. Dissolved sulfide distributions in the water column and sediment pore waters of the Santa Barbara Basin. Geochim. Cosmochim. Acta 63, 2199–2209 (1999).

    Article  ADS  CAS  Google Scholar 

  9. Soutar,A. & Crill,P. A. Sedimentation and climatic patterns in the Santa Barbara Basin during the 19th and 20th centuries. Geol. Soc. Am. Bull. 88, 1161–1172 (1977).

    Article  ADS  Google Scholar 

  10. Fenchel,T. et al. Microbial diversity and activity in a Danish fjord with anoxic deep water. Ophelia 43, 45–100 (1995).

    Article  Google Scholar 

  11. Simpson,A. G. B. et al. The ultrastructure and systematic position of the euglenozoon Postgaardi mariagerensis̀, Fenchel et al. Arch. Protistenkd. 147, 213–225 (1996/1997).

    Article  Google Scholar 

  12. Esteban,G., Fenchel,T. & Finlay,B. Diversity of free-living morphospecies in the ciliate genus Metopus. Arch. Prostistenkd. 146, 137–164 (1995).

    Article  Google Scholar 

  13. Fenchel,T. & Finlay,B. J. (eds) Ecology and Evolution in Anoxic Worlds (Oxford Univ. Press, Oxford, 1995).

    Google Scholar 

  14. Ott,J. A., Novak,R., Schiemer,F., Hentschel,U., Nebelsick,M. & Polz,M. Tackling the sulfide gradient—a novel strategy involving marine nematodes and chemoautotrophic ectosymbionts. PSZNI Mar. Ecol. 12, 261–279 (1991).

    Article  Google Scholar 

  15. Buck,K. R. & Barry,J. P. Monterey Bay cold seep infauna: quantitative comparison of bacterial mat meiofauna with non-seep control sites. Cahiers de Biologie Marine 39, 333–335 (1998).

    Google Scholar 

  16. Bernard,C. & Fenchel,T. Mats of colourless sulphur bacteria: II. Structure, composition of biota and successional patterns. Mar. Ecol. (Prog. Ser.) 128, 171–179 (1995).

    Article  ADS  Google Scholar 

  17. Epstein,S. Simultaneous enumeration of protozoa and micrometazoa from marine sandy sediments. Aquat. Microb. Ecol. 9, 219–227 (1995).

    Article  Google Scholar 

  18. Alongi,D. M. The distribution and composition of deep-sea microbenthos in a bathyal region of the western Coral Sea. Deep-Sea Res. 34, 1245–1254 (1987).

    Article  ADS  CAS  Google Scholar 

  19. Saphonov,M. V. & Tzetlin,A. B. Nerillidae (Annelida: Polychaeta) from the White Sea, with description of a new species of Micronerilla Jouin. Ophelia 47, 215–226 (1997).

    Article  Google Scholar 

  20. Bernhard,J. M. Microaerophilic and facultative anaerobic benthic foraminifera: a review of experimental and ultrastructural evidence. Rev. Paleobiol. 15, 261–275 (1996).

    Google Scholar 

  21. Lee,J. J. & Anderson,O. R. (eds) Biology of Foraminifera (Academic, London, 1991).

    Google Scholar 

  22. Anderson,O. R. & Matsuoka,A. Endocytoplasmic microalgae and bacteroids within the central capsule of the radiolarian Dictyocoryne truncatum. Symbiosis 12, 237–247 (1992).

    Google Scholar 

  23. Richardson,S. L. & Rützler,K. Bacterial endosymbionts in the agglutinating foraminiferan Spiculidendron corallicolum Rützler and Richardson, 1996. Symbiosis 26, 299–312 (1999).

    Google Scholar 

  24. Bernhard,J. M. & Bowser,S. S. Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology. Earth Sci. Rev. 46, 149–165 (1999).

    Article  ADS  CAS  Google Scholar 

  25. Desbruyères,D. et al. Biology and ecology of the “Pompeii worm” (Alvinella pompejana Desbruyères and Laubier), a normal dweller of an extreme deep-sea environment: a synthesis of current knowledge and recent developments. Deep-Sea Res. II 45, 383–422 (1998).

    Article  ADS  Google Scholar 

  26. Stolz,J. F., Chang,S-B. R. & Kirschvink,J. L. Magnetotactic bacteria and single-domain magnetite in hemipelagic sediments. Nature 321, 849–851 (1986).

    Article  ADS  Google Scholar 

  27. Kennett,J. P., Baldauf,J. G. & Lyle,M. (eds) Proceedings of the Ocean Drilling Program, Scientific Results Vol. 146 Part 2 (Ocean Drilling Program, College Station, TX, 1995).

    Google Scholar 

  28. Diaz,R. J. & Rosenberg,R. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33, 245–303 (1995).

    Google Scholar 

  29. Broenkow,W. W. & Cline,J. D. Colorimetric determination of dissolved oxygen at low concentrations. Limnol. Oceanogr. 14, 450–454 (1969).

    Article  ADS  CAS  Google Scholar 

  30. Starink,M. et al. Quantitative centrifugation to extract benthic protozoa from freshwater sediments. Appl. Environ. Microbiol. 60, 167–173 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the captain, crew and scientific parties of the RV Robert Gordon Sproul; C. Bernard, G. Esteban, T. Fenchel and A. Simpson for flagellate and ciliate identifications; W. Fowle, H. Ghiradella, L. Harris, C. Jouin-Toulmond, M. Müller, A. Todaro, A. Vanreusel and M. Vincx for assistance with metazoan identifications; E. Braun-Howland and A. Marcario for valuable discussions; A. van Geen for two collecting opportunities; and T. Fenchel for comments on the manuscript. The Wadsworth Center's Electron Microscopy Core and NIH Biotechnological Resource Grant supporting the Biological Microscopy and Image Reconstruction Resource are acknowledged. This work was supported by USC's Career Development Professorship Program, the Packard Foundation and grants from NSF (PEET Systematics to M.A.F., Polar Programs to S.S.B., Ocean Sciences to J.M.B.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joan M. Bernhard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bernhard, J., Buck, K., Farmer, M. et al. The Santa Barbara Basin is a symbiosis oasis. Nature 403, 77–80 (2000). https://doi.org/10.1038/47476

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/47476

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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