Riftia pachyptila Symbiosis with Thioautotrophic Bacteria

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Introduction

The functioning of an ecosystem depends upon the presence of organisms that can fix carbon dioxide to organic carbon. In environments without solar radiation, primary production depends on the processes of chemolithoautotrophs – chemosynthetic organisms which oxidize inorganic compounds to synthesize the NADPH and ATP needed to reduce carbon dioxide. The Riftia pachyptila, commonly known as the giant tube worm, has taken advantage of the ability of such chemolithoautotrophs, specifically thioautotrophic bacteria, and serves as a model organism for the study of host-symbiont co-evolution in deep-sea ocean vents 14.


Habitat

Hydrothermal vents occur in fissures on the seafloor, especially around active volcanoes14. Seawater seeps into these vents, circulates within the earth’s crust, and escapes back onto the surface as superheated vent fluid14. This vent fluid, which often reaches 300-400 ̊C in temperature, contains a high concentration of hydrogen sulfide from the reduction of sulfate by geothermal activity and interaction with sulfur-containing rocks such as basalt6. Vent sites are characterized by high acidity (pH 3-6), low oxygen levels, and extremely high temperatures14. In contrast, the ambient water surrounding the vent sites is cold and relatively rich in oxygen14. The Riftia pachyptila thrive at the interface between these two extremities, at a pH of around 6 and a temperature of 40 ̊C14. However, due to the complex interaction between populations of microbial organisms, the vent sites are rarely stable in flow rate, temperature, and sulfide concentrations9,11. To exploit this sporadic environment, both the host and the symbiont have developed interdependencies and have co-evolution.


Thioautotrophic mutualism

Thioautotrophic bacteria obtain energy needed for biosynthesis via sulfide-oxidation, which requires the presence of both sulfur and oxygen14. This poses an interesting challenge in the seafloor habitat, because sulfur and oxygen are distributed in distinctive zones14. High concentrations of dissolved sulfur are only present in extremely hot vent fluid, while oxygen is found in the cold, ambient seawater14. In addition, sulfur reacts spontaneously with oxygen to form oxides, making it even more inaccessible to thioautotrophs14. Although this oxidation process happens at a slower rate than biological fixation of sulfur, it nevertheless decreases its availability10,13. This is why most thioautotrophs are restricted to the interface between the ocean and the atmosphere to compete for binding to available oxygen14. Thioautotroph symbionts, however, have uniquely adapted to their environment byassociating with a protective environment, i.e. a host14. As a result, they are able to occupy a niche far away from the fierce competition happening at the ocean surface.


Acquisition of Thioautotrophs