A marine flatworm/chemoautotrophic bacteria symbiosis

All species of the genus Paracatenula (Catenulida, Platyhelminthes) lack a mouth and the gut is transformed into a strand of tissue containing endocellular bacteria. For one species, Paracatenula ruetzleri, from shallow coral sands in the Caribbean Sea it has been shown that the bacteria, which account for up to 50% of the biomass of the symbiotic consortium, are chemoautotrophic sulphur-oxidizing Alphaproteobacteria. Paracatenula species have been reported from a variety of warm temperate to tropical locations. In this project we propose to study the biogeography, diversity, distribution and aspects of the ecology and evolution of this symbiosis at locations in the Caribbean Sea, the Red Sea, the Indian and Pacific Ocean and the Mediterranean Sea. Both the platyhelminth hosts and the bacteria will be characterized by conventional light microscopy, TEM and several genetic markers. The interactions between the symbiosis partners, namely possible transfer of organic carbon from the chemoautotrophic bacteria to the heterotrophic mouthless host will be studied using inorganic 14C incorporation. Symbiont transmission within the trophosome and between host generations will be studies with in-situ hybridization and immuno-cytochemical markers.

Although marine shallow water sandy bottoms superficially appear desert-like the interstitial space between the sand grains is inhabited by a diversity of bacteria, protozoa and microscopic invertebrates. Among them are mouth and gut-less flatworms belonging to the genus Paracatenula. The worms acquire their food similar to the giant mouth-less tubeworms found at deep ocean hot vents by living in symbiosis with intracellular bacteria that oxidize reduced sulfur compounds. The energy thus obtained is used by the symbionts to fix inorganic carbon into biomass. Due to the high productivity of the symbionts, their hosts can derive all their nutrition from them. Many marine animals belonging to different phyla have been found to live in such a symbiotic association. In contrast to the great diversity of their hosts, however, the diversity of the microbial symbionts was limited to the classes gamma-and epsilon-proteobacteria. The symbionts of Paracatenula however are alpha-proteobacteria. Several other important intracellular symbionts belong to this class, such as the nitrogen-fixing root nodule bacteria of leguminous plants or mitochondria. In addition dangerous pathogens such as the causative agent of epidemic typhus also are alpha-proteobacteria. In recent years several studies have presented evidence that the mechanisms in symbiotic and pathogenic relationships are similar or even identical. Future studies on Paracatenula and its symbionts called Riegeria could give fundamental insights into the mechanisms that have allowed alpha-proteobacteria to establish an intracellular lifestyle independently several times. The symbionts of Paracatenula live in specialized cells called bacteriocytes and account for up to 50 percent of the total biomass of the symbiotic animal/bacteria consortium. That is significantly more than in all other known symbioses between animals and bacteria. Based on gene sequences of the symbionts we estimate the age of the symbiosis to be 500 million years. This makes this symbiosis the oldest known animalbacteria association. The phylogenies of hosts and symbionts are absolutely congruent. This means that the worms have been passing on their symbionts to their offspring in every generation, without any symbiont switches for the last 500 million years. This has been possible through the preferred mode of reproduction, namely asexual fission (Paratomy). In this way symbionts are transferred to new individuals without even leaving the bacteriocytes of the host.