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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.

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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.

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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.

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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.

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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

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Correspondence to Nicole Dubilier.

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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

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