Until the late 1970s, scientists were convinced that all life on earth depended largely on the sun for energy. However, when geologists stumbled on the first deep-sea hydrothermal vents, at depths well beyond light penetration, they discovered thriving ecosystems powered not by sunlight, but chemosynthesis. Peter Girguis explains that symbiotic organisms living by the hydrothermal vents derive energy by chemosynthesis of toxic sulphide compounds released from the vents, to power the conversion of carbon dioxide into sugars for consumption by their tubeworm hosts. The environment inhabited by these symbiotic creatures is also incredibly dynamic, with mixing between the icy ocean waters and scalding deep-sea geysers causing sulphide levels to vary from almost zero to several millimolar within a matter of moments. Which made Girguis and James Childress wonder how symbiotic Riftia pachyptilatubeworms sustain some of the highest growth rates ever measured when their energy supply is so variable. Girguis and Childress decided to find out how varying the tubeworm's environment affected the symbiont's metabolism(p. 3516), but first they had to build an oceangoing high pressure respirometer to keep the tubeworms happy onboard ship while they made their sensitive measurements.

Childress and Girguis attached a mass-spectrometer to a high-pressure aquarium, but delivering high-pressure seawater to the high-vacuum mass-spectrometer posed enormous technical challenges. Having successfully plumbed the two together, the team heading out into the Pacific Ocean to collect tubeworms and begin measuring their sulphide, carbon and oxygen uptake rates over a range of physiological conditions.

Recreating the tubeworm's hydrothermal vent environment by bubbling carbon dioxide, hydrogen sulphide and oxygen through seawater before delivering it to the high-pressure aquarium, they supplied the symbionts with oxygen over a range of 40 mmol l-1 to 210 mmol l-1 at fixed sulphide and carbon levels and found that the animal's oxygen consumption rate rose continually as the oxygen supply increased. The team also increased the animal's carbon dioxide supply up to a maximum of 8 mmol l-1, while keeping their sulphide and oxygen levels constant, and found that the animal's carbon consumption rates also increased up to a maximum level. But most importantly, how did the animals respond to fluctuations in their sulphide supply?

Knowing that sulphides come in two forms (toxic H2 S and less toxic HS-), Girguis and Childress measured the tubeworm's sulphide uptake rates by switching between the two forms at pH 5.66 and 7.48 and found that surprisingly the tubeworms were able to take up both forms. They suspect that the toxic H2S form is converted to the safer HS form once in the animal's blood. They also found that the tubeworm's uptake rate increased as the sulphide and oxygen supplies increased, but dropped dramatically once environmental sulphide levels became dangerously high at 700 mmol l-1.

The most startling results came when the team dropped the tubeworm's sulphide supply to zero, expecting to see carbon uptake drop too. However the symbionts continued to take up carbon dioxide and synthesise sugars, even though they had lost their power source. The team suspects that the tubeworm had stored enough sulphide in its body to keep its symbiotic lodger well supplied when sulphide in the environment became scarce. Which probably explains why Riftia thrives its turbulent surroundings, using its body as a buffer to protect its bacterial lodger from environmental fluctuations.

Girguis, P. R. and Childress, J. J. (
2006
). Metabolite uptake, stoichiometry and chemoautotrophic function of the hydrothermal vent tubeworm Riftia pachyptila: responses to environmental variations in substrate concentrations and temperature.
J. Exp. Biol.
209
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-3528.