Symbiosis of gutless Oligochaetes


Coordination: Christian Lott

They have no mouth, no intestine, no anus, no nephridia. They live in shallow sandy bottoms in tropical and subtropical seas and they have a very strange way of living: underneath their skin they harbor up to 6 different species of bacteria that apparently assure nutrition as well as detoxification functions to their animal host.

In 1998 two species of the genus Olavius were found, the first record of this group for the Mediterranean Sea. Both species are flashy white, about 2 cm long and 100 to 200 µm thick. The new species Olavius ilvae is less abundant than Olavius algarvensis, which was found already at the Atlantic coast of Portugal some years before. The most important study site where at least 4 species occur is the Bay of Sant'Andrea in the Northwest of Isola d'Elba, but new findings of more gutless oligochaete species were recently made in the protected area around the neighboring Isola di Pianosa.

"Our worms" became famous after the discovery of the relation between bacteria and host that seems to be linked to the utilization and internal recycling of different sulfur species. While one group of bacteria is able to fix autotrophically CO2, the other bacteria produce sulfide by using sulfate from the surrounding seawater.

The hypothesis is that by migrating between the oxygen-rich and oxygen-depleted zone in the sediment the worm is able to reload its eco-physiological battery and profits from the biomass built up by its bacterial symbionts.

The molecular aspects of this hypothesis are studied by Dr. Nicole Dubilier and her symbiosis group at the Max-Planck-Institute for Marine Microbiology in Bremen. The underlying metabolic pathways of this multiple symbiosis could be put in a model (Dubilier, et al., 2001).

During the first big metagenome study of a multiple symbiosis, in cooperation with Dr. Tanja Woyke at the Joint Genome Institute, a deeper insight was gained into the physiological potential of the bacterial partners (Woyke, et al., 2006). The study of the actually expressed genes, the logical consequence, is conducted by Manuel Kleiner (University of Greifswald and Symbiosis Group, MPI Bremen) in a big metaproteomic project.


The microsensor group of Dr. Dirk de Beer at MPI studies the biogeochemistry of the habitat. To be able to link informations from the genome analysis with the way of living of the worms, Christian Lott (HYDRA/MPI Bremen) is studying these topics on-site:

- Biogeochemistry in the natural environment, especially the search for the final electron acceptor for the oxidation of the sulfide;
- Population dynamics and distribution of the several species;
- Eco-physiology of symbionts and host;
- Transmission of the symbionts from parents to their offspring. This aspect is meanwhile studied by Cécilia Wentrup.



Dr. Nicole Dubilier, Dr. Caroline Rühland, Dr. Claudia Bergin, Cécilia Wentrup, Manuel Kleiner, Christian Lott (Symbiosis Group, Max-Planck-Institute for Marine Microbiology, Bremen): Molecular Ecology
Dr. Dirk de Beer, Dr. Miriam Weber, Dr. Lubos Polerecky (Microsensor Group, Max-Planck-Institute for Marine Microbiology, Bremen): Biogeochemistry, Microsensors, Modeling
Stefan Häusler (University of Heidelberg, MPI Bremen, HYDRA):Physiology
Dr. Tanja Woyke (Joint Genome Institute, Berkeley, USA): Metagenomics
Prof. Dr. Thomas Schweder, Prof. Dr. Michael Hecker, Manuel Kleiner (ZIK und Uni Greifwald): Metaproteomics
Prof. Dr. Olav Giere (Uni Hamburg): Meiofauna
Prof. Dr. Christer Erséus (Uni Göteborg/Schweden): Taxonomy and phylogeny of gutless Oligochaets
Prof. Dr. Georg Fuchs, Jan Zarzycki (Uni Freiburg): Enzyme activity
Dr. Michael Lalk, Manuel Liebeke (Pharmazeutische Biologie, Uni Greifswald): organic compounds within the porewater
Dr. Nathan C. VerBerkmoes (Oak Ridge National Laboratory, Tennessee, USA): Metaproteomics



Giere O & Ersèus C (2000):
Taxonomy and new bacterial symbioses of gutless marine Tubificidae (Annelida, Oligochaeta) from the Island of Elba (Italy).
Org. Divers. Evol. 2:289-297

Dubilier N, et al. (2001):
Endosymbiotic sulphate-reducing and sulphur-oxidizing bacteria in an oligochaete worm.
Nature 411:298-302

Miriam Perner (2003):
Biogeochemische und mikrobiologische Charakterisierung mariner Sedimente vor Elba – ein Beitrag zur ökosystemaren Analyse bakteriensymbiontischer Oligochaeten.
Diplomarbeit, Uni Hamburg

Woyke, et al. (2006):
Metagenomics of microbial symbionts in a gutless worm.
Nature 443:950-955

Weber, (2007):
In situ applications of a new diver-operated motorized microsensor profiler.
Environmental Science and Technology, 41 (17): 6210-6215

Ruehland C, Blazejak A, Lott C, Loy A, Erséus C, Dubilier N. (2008):
Multiple bacterial symbionts in two species of co-occurring gutless marine
worms from Mediterranean sea grass sediments.
Environ. Microbiol. 10: 3404-3416

Kleiner M, Woyke T, Ruehland C, Dubilier N. In press.
The Olavius algarvensis metagenome revisited: lessons learned from the analysis
of the low diversity microbial consortium of a gutless marine worm.
In: Handbook of Molecular Microbial Ecology II; Metagenomics in Different Habitats. Ed: de Bruijn FJ. Wiley/Blackwell.

to read more about chemosynthetic symbioses:

Dubilier N, Bergin C, Lott (2008):
Symbiotic diversity in marine animals: the art of harnessing chemosynthesis.
Nature Rev. Mic. 6:725-740