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.

Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm

Nature volume 411, pages 298–302 (2001)Cite this article

Abstract

Stable associations of more than one species of symbiont within a single host cell or tissue are assumed to be rare in metazoans because competition for space and resources between symbionts can be detrimental to the host1. In animals with multiple endosymbionts, such as mussels from deep-sea hydrothermal vents2 and reef-building corals3, the costs of competition between the symbionts are outweighed by the ecological and physiological flexibility gained by the hosts. A further option for the coexistence of multiple symbionts within a host is if these benefit directly from one another, but such symbioses have not been previously described. Here we show that in the gutless marine oligochaete Olavius algarvensis, endosymbiotic sulphate-reducing bacteria produce sulphide that can serve as an energy source for sulphide-oxidizing symbionts of the host. Thus, these symbionts do not compete for resources but rather share a mutalistic relationship with each other in an endosymbiotic sulphur cycle, in addition to their symbiotic relationship with the oligochaete host.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Transmission electron micrograph of bacterial endosymbionts in O. algarvensis.
Figure 2: Phylogenetic relationships of the O. algarvensis symbionts based on maximum likelihood analyses.
Figure 3: Fluorescence in situ hybridization of endosymbionts in O. algarvensis with oligonucleotide probes labelled with fluorochromes.
Figure 4: Model of the endosymbiotic sulphur cycle in O. algarvensis showing syntrophic cycling of oxidized and reduced sulphur compounds between the sulphate-reducing and sulphide-oxidizing symbionts.

Accession codes

Accessions

GenBank/EMBL/DDBJ

Data deposits

GenBank accession numbers: 16S rRNA: γ-Proteobacteria symbiont AF328856, δ-Proteobacteria symbiont AF328857; DSR: δ-Proteobacteria symbiont AF244995, D. variabilis AF191907.

References

  1. Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution (Oxford Univ. Press, Oxford 1995).

    Google Scholar 

  2. Distel, D. L., Lee, H. K.-W. & Cavanaugh, C. M. Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proc. Natl Acad. Sci. USA 92, 9598– 9602 (1995).

    Article  ADS  CAS  Google Scholar 

  3. Rowan, R., Knowlton, N., Baker, A. & Jara, J. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265– 266 (1997).

    Article  ADS  CAS  Google Scholar 

  4. Giere, O., Erséus, C. & Stuhlmacher, F. A new species of Olavius (Tubificidae, Phallodrilinae) from the Algarve Coast in Portugal, the first East Atlantic gutless oligochaete with symbiotic bacteria. Zool. Anzeiger 237, 209– 214 (1998).

    Google Scholar 

  5. Giere, O. & Langheld, C. Structural organisation, transfer and biological fate of endosymbiotic bacteria in gutless oligochaetes. Mar. Biol. 93, 641– 650 (1987).

    Article  Google Scholar 

  6. Giere, O., Nieser, C., Windoffer, R. & Erséus, C. A comparative structural study on bacterial symbioses of Caribbean gutless Tubificidae (Annelida, Oligochaeta). Acta Zool. 76, 281– 290 (1995).

    Article  Google Scholar 

  7. Dubilier, N. et al. Phylogenetic diversity of bacterial endosymbionts in the gutless marine oligochaete Olavius loisae (Annelida). Mar. Ecol. Prog. Ser. 178, 271– 280 (1999).

    Article  ADS  Google Scholar 

  8. Dubilier, N., Giere, O., Distel, D. L. & Cavanaugh, C. M. Characterization of chemoautotrophic bacterial symbionts in a gutless marine worm (Oligochaeta, Annelida) by phylogenetic 16S rRNA sequence analysis and in situ hybridization. Appl. Environ. Microbiol. 61, 2346– 2350 (1995).

    Article  ADS  CAS  Google Scholar 

  9. Krieger, J., Giere, O. & Dubilier, N. Localization of RubisCO and sulfur in endosymbiotic bacteria of the gutless marine oligochaete Inanidrilus leukodermatus (Annelida). Mar. Biol. 137, 239– 244 (2000).

    Article  CAS  Google Scholar 

  10. Vetter, R. D. & Fry, B. Sulfur contents and sulfur-isotope compositions of thiotrophic symbioses in bivalve molluscs and vestimentiferan worms. Mar. Biol. 132, 453– 460 (1998).

    Article  CAS  Google Scholar 

  11. Kuhnigk, T., Branke, J., Krekeler, D., Cypionka, H. & König, H. A feasible role of sulfate-reducing bacteria in the termite gut. System. Appl. Microbiol. 19, 139– 149 (1996).

    Article  CAS  Google Scholar 

  12. Morvan, B., Bonnemoy, F., Fonty, G. & Gouet, P. Quantitative determination of H2-utilizing acetogenic and sulfate-reducing bacteria and methanogenic archaea from digestive tracts of different mammals. Curr. Microbiol. 32, 129– 133 (1996).

    Article  CAS  Google Scholar 

  13. Fenchel, T. & Ramsing, N. B. Identification of sulphate-reducing ectosymbiotic bacteria from anaerobic ciliates using 16S rRNA binding oligonucleotide probes. Arch. Microbiol. 158, 394– 397 (1992).

    Article  CAS  Google Scholar 

  14. Bussmann, I. & Reichardt, W. Sulfate-reducing bacteria in temporarily toxic sediments with bivalves. Mar. Ecol. Prog. Ser. 78, 97– 102 (1991).

    Article  ADS  Google Scholar 

  15. Cottrell, M. T. & Cary, C. S. Diversity of dissimilatory bisulfite reductase genes of bacteria associated with the deep-sea hydrothermal vent polychaete Alvinella pompejana. Appl. Environ. Microbiol. 65, 1127– 1132 (1999).

    Article  ADS  CAS  Google Scholar 

  16. Wagner, M., Roger, A. J., Flax, J. L., Brusseau, G. A. & Stahl, D. A. Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J. Bacteriol. 180, 2975– 2982 (1998).

    Article  CAS  Google Scholar 

  17. Dubilier, N., Giere, O. & Grieshaber, M. K. Morphological and ecophysiological adaptations of the marine oligochaete Tubificoides benedii to sulfidic sediments. Am. Zool. 35, 163– 173 (1995).

    Article  CAS  Google Scholar 

  18. Grieshaber, M. K., Hardewig, I., Kreutzer, U. & Pörtner, H.-O. Physiological and metabolic responses to hypoxia in invertebrates. Rev. Physiol. Biochem. Pharmacol. 125, 43– 147 (1994).

    CAS  PubMed  Google Scholar 

  19. Barton, L. L. Sulfate-Reducing Bacteria (Plenum, New York, 1995).

    Book  Google Scholar 

  20. Jørgensen, B. B. A comparison of methods for the quantification of bacterial sulfate reduction in coastal marine sediments. III. Estimation from chemical and bacteriological field data. Geomicrobiol. J. 1, 49– 64 (1978).

    Article  Google Scholar 

  21. Sahm, K., MacGregor, B. J., Jørgensen, B. B. & Stahl, D. A. Sulphate reduction and vertical distribution of sulphate-reducing bacteria quantified by rRNA slot-blot hybridization in a coastal marine sediment. Environ. Microbiol. 1, 65– 74 (1999).

    Article  CAS  Google Scholar 

  22. Canfield, D. E. & Des Marais, D. J. Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim. Cosmochim. Acta 57, 3971– 3984 (1993).

    Article  ADS  CAS  Google Scholar 

  23. Giere, O., Conway, N. M., Gastrock, G. & Schmidt, C. ‘Regulation’ of gutless annelid ecology by endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 68, 287– 299 (1991).

    Article  ADS  Google Scholar 

  24. van den Ende, F. P., Meier, J. & van Gemerden, H. Syntrophic growth of sulfate-reducing bacteria and colorless sulfur bacteria during oxygen limitation. FEMS Microbiol. Ecol. 23, 65– 80 (1997).

    Article  CAS  Google Scholar 

  25. Cline, J. D. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14, 454– 458 (1969).

    Article  ADS  CAS  Google Scholar 

  26. Fossing, H. & Jørgensen, B. B. Measurements of bacterial sulfate reduction in sediments: Evaluation of a single-step chromium reduction method. Biogeochemistry 8, 205– 222 (1989).

    Article  CAS  Google Scholar 

  27. Ferdelman, T. G. et al. Sulfate reduction and methanogenesis in a Thioploca-dominated sediment off the coast of Chile. Geochim. Cosmochim. Acta 61, 3065– 3079 (1997).

    Article  ADS  CAS  Google Scholar 

  28. Crank, J. The Mathematics of Diffusion (Oxford Univ. Press, New York, 1975).

    MATH  Google Scholar 

Download references

Acknowledgements

We thank F. Widdel and B. Barker Jørgensen for reviewing this manuscript; E. Llobet-Brossa and A. Boetius for discussions; the Hydra Institute for Marine Sciences on Elba for logistical support during collection of the worms; and J. Wulf, D. Lange, G. Eickert and A. Eggers for technical support. The Max-Planck Society and the German Research Foundation (DFG) provided financial support.

Author information

Authors and Affiliations

  1. Max Planck Institute of Marine Microbiology, Celsiusstrasse 1, Bremen, D-28359, Germany

    Nicole Dubilier, Caroline Mülders, Tim Ferdelman, Dirk de Beer, Annelie Pernthaler & Rudolf Amann

  2. Department of Microbiology, Technical University of Munich, Freising, D-85350, Germany

    Michael Klein & Michael Wagner

  3. Department of Invertebrate Zoology, Swedish Museum of Natural History, Stockholm, S-10405, Sweden

    Christer Erséus

  4. Zoological Institute and Zoological Museum, University of Hamburg, Hamburg, D-20146, Germany

    Frank Thiermann, Jens Krieger & Olav Giere

Authors
  1. Nicole Dubilier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caroline Mülders
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tim Ferdelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dirk de Beer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Annelie Pernthaler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Klein
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Christer Erséus
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Frank Thiermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jens Krieger
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Olav Giere
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Rudolf Amann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicole Dubilier.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dubilier, N., Mülders, C., Ferdelman, T. et al. Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411, 298–302 (2001). https://doi.org/10.1038/35077067

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35077067

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

Advanced 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