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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

View larger version (21K): [in a new window]   Fig. 1. Diagram of the custom-built polysulfone gas extractor. Seawater is directed by a stream selection valve into the extractor, where it is mixed with phosphoric acid, bubbled with helium and sent for analysis by a quadropole mass spectrometer. The liquid level is maintained between two quartz optical liquid detectors. The seawater/acid mixture is periodically drained off through the drain port when its level reaches the top detector.

View larger version (24K): [in a new window]   Fig. 2. Plots of proton elimination rate (µequiv g-1 h-1) versus (A) total sulfide uptake rate (µmol H2S g-1 h-1) and (B) total sulfide concentration (µmol l-1) by Riftia pachyptila. The regression lines for the relationship between proton elimination rate and total sulfide uptake rate (A), and the relationship between proton elimination rate and environmental total sulfide (B) are highly significant (P<0.0001 and P<0.005; ANOVA). In this experiment, the total dissolved sulfide concentration in the seawater was increased incrementally from 100 to 408 µmol l-1, while sulfide uptake and proton elimination rates were determined simultaneously. All other conditions were held under approximately in situ conditions (CO2=5.5 mmol l-1, [O2]=250 µmol l-1, [NO3-]=40-65 µmol l-1, pH 6.2; temperature, 12°C, pressure, 27.5 MPa). Rates are expressed in terms of wet mass.

View larger version (19K): [in a new window]   Fig. 3. Effects of decreased environmental sulfide on metabolite uptake rates (A,B) (µmol g-1 h-1) and proton elimination rates (C) (µequiv g-1 h-1) by Riftia pachyptila. Worms were kept at in situ conditions (see Materials and methods) in the aquaria until autotrophy. Gaseous hydrogen sulfide flow into the equilibration column was turned off, and the aquarium seawater sulfide concentrations dropped to levels below our limits of detection (approximately 5 µmol l-1; Childress et al., 1984). The arrow indicates the time at which gaseous sulfide flow was stopped in the equilibration column. Rates are expressed in terms of wet mass. H2S, total sulfide.

View larger version (17K): [in a new window]   Fig. 4. (A-C) Plots of proton elimination rates (µequiv g-1 h-1) versus total inorganic carbon uptake rates (µmol g-1 h-1) by Riftia pachyptila during exposure to three different seawater inorganic carbon regimes. Worms were maintained for several hours to establish autotrophy. Total dissolved seawater inorganic carbon concentration was then varied to produce (A) continuously increasing, (B) steady or (C) continuously decreasing environmental inorganic carbon concentrations, while proton elimination rates were measured. All other conditions were held under approximately in situ conditions (see Materials and methods). Rates are expressed in terms of wet mass.

View larger version (16K): [in a new window]   Fig. 5. Plots of the effects of amiloride on metabolite uptake rates (A—C) (µmol g-1 h-1) and proton elimination rate (D) (µequiv g-1 h-1) by Riftia pachyptila. Worms were maintained under in situ conditions (see Materials and methods) until they exhibited signs of autotrophy. The arrow denotes the time at which amiloride was added to the seawater to achieve a final concentration of 1 mmol l-1. A flow of fresh seawater was maintained through the aquaria after exposure to amiloride. Rates are expressed in terms of wet mass.