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Abstract

A fascinating variety of marine invertebrates occur in dense assemblages in organically enriched sulfidic environments ranging from deep-sea hydrothermal vent and cold seeps, to estuarine mudflats. These animals are exposed to the highly toxic, yet energy-rich molecule, hydrogen sulfide and fall into two groups: those containing symbiotic bacteria which utilize sulfide as an energy source (chemosynthesis) and the non-chemosynthetic animals that feed and metabolize in a traditional manner. In both cases, physiological function is maintained during toxic exposure by sulfide detoxification, allowing colonization of what would be extremely hostile environments to most marine organisms.

At 2500 meters in depth on the East Pacific Rise, the dynamic, volcanic hydrothermal vent sites are home to dramatic communities of robust invertebrates who rely on the sulfide-laden fluids issuing rapidly though cracks in the ocean floor. The discovery of these remote habitats and their unusual fauna 20 years ago altered scientistsí assumption that all ecosystems were dependent upon sunlight and photosynthesis as the basis of the food chain. Here chemoautotrophic endosymbiont-harboring worms, clams and mussels utilize the sulfide present in hydrothermal fluids to fuel bacterial metabolism and ultimately, production of food stuffs. Most completely lack digestive systems and feeding structures. In order to exploit this potent energy source, tolerance of toxic sulfide is achieved through binding to blood-borne components in chemosynthetic vestimentiferans and vesicomyid clams, and is particularly well characterized for the tube worm Riftia pachyptila. These worms simultaneously transport sulfide to the internal bacterial symbionts, as well as protect animal tissue against toxicity. Much of the vent environment is dominated by clusters of these meter long, bright red tubeworms, which constitute a huge biomass for such a remote, deep sea environment.

At 600 meters in the Gulf of Mexico, chemosynthetic communities congregate around naturally seeping pools of sulfide, methane and hypersaline brine. This habitat is less dynamic than the vents, but presents many of the same physiological challenges. Characterized by chemosynthetic mussels that utilize methane as their inorganic energy supply, and longer, but more delicate tubeworm relatives of the vent species, they provide a different suite of environmental parameters and different physiological adaptations to their unique set of problems. A group of scientists including myself and SFSU research associate Dr. David Julian, on a recent expedition to this seep environment, discovered an unusual polychaete worm densely colonizing mounds of frozen methane. These mushroom shaped mounds are approximately 2 by 3 meters in size and are covered with individual burrows, each inhabited by a worm. This previously undescribed association has stimulated a flurry of research activities and hypotheses addressing the biology and physiology of these unusual animals.

In our own backyard, the California intertidal mudflat harbors dense assemblages of burrowing invertebrates that are not readily apparent to the casual observer. Sulfide detoxification in these non-chemosynthetic, burrowing marine animals is essential to their survival, but they do not require an internal supply of sulfide. Our lab has focused on the physiology of the echiuran worm Urechis caupo, an estuarine worm exposed to toxic sulfide when its normally well ventilated burrow is exposed during low tide on the marine mudflat. Although sulfide freely penetrates the epithelial surfaces of the body, the animal tolerates moderate sulfide levels through a combination of adaptations that protect the body tissues and internal fluids. Sulfide oxidation does not appear to provide a significant energetic contribution to the overall metabolism of this animal. Rather, these mechanisms allow populations of this filter-feeding worm to flourish in its nutrient-rich, sulfidic environment.

Various sulfide detoxification strategies have been described to date for marine animals from a wide range of sulfidic environments. Sulfide tolerant animal appear to have evolved unique suites of adaptations associated with their particular habitat and these mechanisms allow large communities of animals to flourish in habitats that would typically be considered inhospitable to life--remote, oxygen limited and extremely toxic.


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