Biochemical and enzymological aspects of the symbiosis between the deep‐sea tubeworm Riftia pachyptila and its bacterial endosymbiont

Abstract

Riftia pachyptila (Vestimentifera) is a giant tubeworm living around the volcanic deep-sea vents of the East Pacific Rise. This animal is devoid of a digestive tract and lives in an intimate symbiosis with a sulfur-oxidizing chemoautotrophic bacterium. This bacterial endosymbiont is localized in the cells of a richly vascularized organ of the worm: the trophosome. These organisms are adapted to their extreme environment and take advantage of the particular composition of the mixed volcanic and sea waters to extract and assimilate inorganic metabolites, especially carbon, nitrogen, oxygen and sulfur. The high molecular mass hemoglobin of the worm is the transporter for both oxygen and sulfide. This last compound is delivered to the bacterium which possesses the sulfur oxidizing respiratory system, which produces the metabolic energy for the two partners. CO 2 is also delivered to the bacterium where it enters the Calvin-Benson cycle.Some of the resulting small carbonated organic molecules are thus provided to the worm for its own metabolism. As far as nitrogen assimilation is concerned, NH 3 can be used by the two partners but nitrate can be used only by the bacterium. This very intimate symbiosis applies also to the organization of metabolic pathways such as those of pyrimidine nucleotides and arginine. In particular, the worm lacks the first three enzymes of the de novo pyrimidine biosynthetic pathways as well as some enzymes involved in the biosynthesis of polyamines. The bacterium lacks the enzymes of the pyrimidine salvage pathway. This symbiotic organization constitutes a very interesting system to study the molecular and metabolic basis of biological adaptation.

Organisms of deep sea hydrothermal vents as a source for studying adaptation and evolution

“…The resulting acidic solution, containing metals (Fe, Mn, Zn, Cu ... ) and reduced sulfur compounds such as sulfides and HzS, percolates up to the sea floor where it mixes with the cold surrounding ocean water (4°C), forming mineral deposits and different types of vents (Tunnicliffe et al, 1998;Zierenberg et al, 2000). These chemicals provide a source of energy and nutrients to chemoautotrophic and other organisms present in this environment (Felbeck, 1981;Felbeck et al, 1981;Cavanaugh et al, 1981;Gaill, 1993;Fisher, 1996;Minic and Herve, 2004;Minie et al, 2006). Organisms include a large variety of microorganisms (Eubacteria, Archaea, mainly extremophiles) and more than five hundred animal species from twelve different phyla (Desbruyeres et al, 2006).…”

“…They could be an example of primary endosymbioses in progress, giving rise to thiotrophic Eukarya (Childress and Fischer, 1992;Lallier, 2006). Various physiological processes of these symbiotic adaptations have been studied and interesting results have been obtained concerning the metabolic adaptation of the host and its endosymbiont, in particu lar for Riftia pachyptila (Minic and Herve, 2004).…”

“…1) (Minic and Herve, 2004). It is a giant tube worm (up to 1.5 m long) and very common on the East-Pacific Rise where it lives in clusters in the immediate vicinity of the vents.…”

“…This sack contains symbiotic bacteria that provide nutrition to the worm. The worm has no mouth, eyes, or stomach (Minic and Herve, 2004). Riftia reproduce by sexual reproduction, since there are both male and female organisms (Bright and Giere, 2005).…”

Proteomic Studies of the Effects of Different Stress Conditions on Central Carbon Metabolism in Microorganisms

“…Some organisms are well adapted to an environment that for others can be considered extreme. For example, the environment of deep sea hydrothermal vents is characterized by high temperature, high pressure, chemical toxicity, acidic pH and limited light, yet a variety of microorganisms and many animal species are specifically adapted to this hostile environment [24][25][26]. Each particular species can adapt and grow optimally under a very specific set of environmental conditions [27].…”