Trophosome Evolution in siboglinid symbioses

The monophyletic family of Siboglinidae (Polychaeta), existing in different extreme and hostile deep-sea habitats from hydrothermal vents, over cold seeps to whale falls, is one of the most exciting example of marine microbial symbiosis. In contrast to other non-symbiotic polychaete relatives, siboglinids formed bacterial symbioses allowing them to survive and prosper in these highly toxic, sulfide-rich environments. Apparently the evolution of this taxon involved the capability of the hosts to establish endosymbiosis in a variety of tissues leading to tightly nutritional associations, the loss of a functioning digestive system, and the transformation of host morphology to serve this symbiosis. However, several pathways must have led to this successful adaptation as reflected in the astonishing variety of siboglinid body plans. Once the symbiont housing organ, the trophosome, is established, no further symbiont migration is found within the hosts. Thus, we assume that only a tissue unspecific, widespread symbiosis in the last common stem species of siboglinids allowed for the evolution of several pathways of trophosome development. However, to date the infection process with bacteria leading to trophosome development is only known in one group of siboglinids, the Vestimentiferans. Thus, in this proposed study the infection process, anatomy and organization of the trophosomes in the sister groups of Vestimentiferans, Sclerolinum from the hydrocarbon seeps of the Gulf of Mexico and the recently discovered Osedax from whale falls off the coast of California, will be investigated using ultrastructural, molecular, and immunohistochemical techniques to elucidate not only the specific symbioses but also to extend our knowledge on microbial symbiosis from beneficial to pathogen associations.

Symbiosis, the living together of dissimilar organism, is a basic principal of life. Plants, fungi, and animals have evolved from symbiosis. The majority of organisms continue to depend on symbiotic interactions. In the marine polychaetes, the small group of Siboglinidae, comprised of frenulates, vestimentiferans, Sclerolinum, and Osedax live in symbiosis with bacteria, allowing them to thrive in extreme environments such as the hydrothermal vents, hydrocarbon seeps, and whale and wood falls. They developed a symbiont-housing organ, the trophosome, and reduced their entire digestive system. To understand the evolution of the trophosome, the adult organization of two genera Sclerolinum and Osedax, and the larvae of vestimentiferans were studied in detail in the project using electron microscopy, immunohistochemistry, Raman microspectroscopy, and molecular methods. The trophosome of Sclerolinum develops from tissue surrounding the gut similar to vestimentiferans. In Osedax it develops in the muscle tissue of the skin, while in frenulates the gut transforms into the trophosome. Growth of the trophosome in these sessile animals is accomplished by proliferation of bacteriocytes containing the symbionts according to the different habitats they inhabit. At hydrothermal vents, where vestimentiferans anchor the posterior end to the basalt from which vent fluid emerges, proliferation is from the center of lobules to the periphery leading to a multi-lobed organ. In Sclerolinum, which extends with its anterior end above the sediment surface of seeps, but grows into the sediment with its posterior part, proliferation is from the anterior to the posterior of the body. Osedax grows with its posterior body into the whalebone and proliferation is from the posterior to the anterior. While the various trophosomes develop from different tissues in siboglinids, the body region in which these organs develop, the trunk region, is the same. This is based on studies of development of body regions in vestimentiferan larvae, of adult Osedax and Sclerolinum specimens and comparing them to published data on frenulates. Such a situation is quite unique among symbiotic animals, all belonging to a small group of polychaetes, with large implications for their evolution. Further, we found very large sulfur crystals in the trophosome of Sclerolinum. We suggested that the symbionts produce them in access of sulfide and thus help the host to tolerate this toxic chemical. Taking together all new data, we proposed that the stem species of siboglinids lived in deep-sea sediments with a well-developed oxic-sulfidic interface. They associated with sulfur bacteria, which spread in many host tissues but were restricted to the trunk. These bacteria detoxified sulfide for the host and nourished the host so that the digestive system could be entirely reduced. From such ecosystem they spread to hydrocarbon seeps, hydrothermal vents, and whale and wood falls, and in each group developed their own, specific trophosome by confining the symbionts to certain tissues.