1. Max Planck Institute of Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany
2. Department of Microbiology, Technical University of Munich, D-85350 Freising, Germany
3. Department of Invertebrate Zoology, Swedish Museum of Natural History, S-10405 Stockholm, Sweden
4. Zoological Institute and Zoological Museum, University of Hamburg, D-20146 Hamburg, Germany

Correspondence to: Nicole Dubilier¹ Correspondence and requests for materials should be addressed to N.D. (e-mail: Email: ndubilie@mpi-bremen.de). GenBank accession numbers: 16S rRNA: -Proteobacteria symbiont AF328856, -Proteobacteria symbiont AF328857; DSR: -Proteobacteria symbiont AF244995, D. variabilis AF191907.

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.