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The Journal of Experimental Biology 205, i1902-i1902 (2002)
© 2002 The Company of Biologists Limited


In this issue

Deep Sea Tubeworms are Champion Proton Pumpers

Kathryn Phillips

kathryn{at}biologists.com


If something smells bad, it's a good rule of thumb that it's toxic too. For most creatures a dose of hydrogen sulphide is enough to kill them, but not vestimentiferan tubeworms that live around hydrothermal vents deep on the ocean floor. They have made a pact with symbiotic bacteria that protect them from the harmful effects of sulphides. The bacteria fuel their metabolism with hydrogen sulphide supplied through the worm's blood. In return the bacteria supply the worms with sugars and ammonia for nourishment. But having turned one of the planet's most toxic environments to its own advantage, the worm runs the risk of being poisoned from the inside by its partner's waste: protons. James Childress and his student Peter Girguis were fascinated by how the worm solves its lodger's waste disposal problem, until they measured the rate that the worm excretes protons into the environment. They discovered that the worm can expend up to half its energy pumping the protons out of its body (p. 3055)!

Living on the ocean floor, vestimentiferan tubeworms really are at the bottom of the food chain, with every species above them in the ocean taking first pickings at the food supply that drifts down from the surface. Faced with the meagre supplies from above, the tubeworms have done away with a digestive tract, and instead rely entirely on the ammonia and sugars synthesisted by their bacterial lodgers. But there is a catch for the worms; the bacteria's waste protons have to be disposed of before they reach life-threatening levels in the worm's long body. Before Childress's team could find out how the worms deal with the proton problem, Girguis had to bring two tubeworm species, and their symbiotic lodgers, to the surface.

Back in the lab, the scientists recreated the worm's high-pressure environment in stainless steel aquaria. Girguis explains that this wasn't straightforward. Although he could keep the worms alive, they didn't flourish, until the aquaria's temperature suddenly rose and the worms began growing as if they were still at the bottom of the ocean. Girguis says that working with the tubeworms taught him `not to make assumptions'.

Girguis supplied individual worms with simulated vent water, and then he slowly increased the amount of H2S while he monitored the water's pH, to see if the worms were excreting protons. Girguis explains that he was only expecting to see a tiny fall in pH, but within minutes of increasing the water's sulphide content, the worms were excreting enough protons to drop the pH from 6.2 to 5.9! When he compared a sulphide-tolerant terrestrial species to the deep-sea worms, the surface dweller could only drop the pH by 0.05 units.

But pumping protons doesn't come cheap; Girguis calculates that the vent worms could be consuming as much as half of their energy simply disposing of the symbiont's waste protons. But he adds that this is an early estimate. He explains that no one has succeeded in culturing the bacteria outside of the vent worm's bodies to accurately measure a symbionts' metabolic rate; which could prove to be yet another misleading low-pressure presumption.


Related articles in JEB:

Effects of metabolite uptake on proton-equivalent elimination by two species of deep-sea vestimentiferan tubeworm, Riftia pachyptila and Lamellibrachia cf luymesi: proton elimination is a necessary adaptation to sulfide-oxidizing chemoautotrophic symbionts
P. R. Girguis, J. J. Childress, J. K. Freytag, K. Klose, and R. Stuber
JEB 2002 205: 3055-3066. [Abstract] [Full Text]  




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