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The Journal of Experimental Biology 205, 3055-3066 (2002)
© 2002 The Company of Biologists Limited

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^1,*, J. J. Childress², J. K. Freytag³, K. Klose² and R. Stuber⁴

¹ Monterey Bay Aquarium Research Institute (MBARI), 7700 Sandholdt Road, Moss Landing, CA 95039, USA
² Department of Ecology, Evolution and Marine Biology, University of California at Santa Barbara, CA 93106, USA
³ Department of Biology, Pennsylvania State University, University Park, PA 16802, USA
⁴ Department of Physics, University of California Santa Barbara, Santa Barbara, CA 93106, USA

^* Author for correspondence (e-mail: girguis{at}mbari.org)

Accepted 9 July 2002

Intracellular symbiosis requires that the host satisfy the symbiont's metabolic requirements, including the elimination of waste products. The hydrothermal vent tubeworm Riftia pachyptila and the hydrocarbon seep worm Lamellibrachia cf luymesi are symbiotic with chemolithoautotrophic bacteria that produce sulfate and protons as end-products. In this report, we examine the relationship between symbiont metabolism and host proton equivalent elimination in R. pachyptila and L. cf luymesi, and the effects of sulfide exposure on proton-equivalent elimination by Urechis caupo, an echiuran worm that lacks intracellular symbionts (for brevity, we will hereafter refer to proton-equivalent elimination as `proton elimination'). Proton elimination by R. pachyptila and L. cf luymesi constitutes the worms' largest mass-specific metabolite flux, and R. pachyptila proton elimination is, to our knowledge, the most rapid reported for any metazoan. Proton elimination rates by R. pachyptila and L. cf luymesi correlated primarily with the rate of sulfide oxidation. Prolonged exposure to low environmental oxygen concentrations completely inhibited the majority of proton elimination by R. pachyptila, demonstrating that proton elimination does not result primarily from anaerobic metabolism. Large and rapid increases in environmental inorganic carbon concentrations led to short-lived proton elimination by R. pachyptila, as a result of the equilibration between internal and external inorganic carbon pools. U. caupo consistently exhibited proton elimination rates 5-20 times lower than those of L. cf luymesi and R. pachyptila upon exposure to sulfide. Treatment with specific ATPase inhibitors completely inhibited a fraction of proton elimination and sulfide and inorganic carbon uptake by R. pachyptila, suggesting that proton elimination occurs in large part via K⁺/H⁺-ATPases and Na⁺/H⁺-ATPases. In the light of these results, we suggest that protons are the primary waste product of the symbioses of R. pachyptila and L. cf luymesi, and that proton elimination is driven by symbiont metabolism, and may be the largest energetic cost incurred by the worms.

Key words: metabolite uptake, proton-equivalent, tubeworm, Riftia pachyptila, Lamellibrachia cf luymesi, Urechis caupo, sulfide, oxidation, chemoautotrophy, symbiosis, vestimentiferan, hydrothermal vent

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