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      Comparison of proton-specific ATPase activities in plume and root tissues of two co-occurring hydrocarbon seep tubeworm species Lamellibrachia luymesi and Seepiophila jonesi

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      Marine Biology
      Springer-Verlag

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          Abstract

          Lamellibrachia luymesi and Seepiophila jonesi are co-occurring species of vestimentiferan tubeworms found at hydrocarbon seepage sites on the upper Louisiana slope of the Gulf of Mexico. Like all vestimentiferans, they rely on internal sulfide-oxidizing symbiotic bacteria for nutrition. These symbionts produce hydrogen ions as a byproduct of sulfide oxidation, which the host tubeworm needs to eliminate to prevent acidosis. The hydrothermal vent tubeworm Riftia pachyptila uses a high activity of P- and V-type H +-ATPases located in its plume epithelium to excrete protons. Unlike R. pachyptila, the seep species grow a posterior root, which they can use in addition to their plumes as a nutrient exchange surface. In this study we measured the ATPase activities of plume and root tissues collected from L. luymesi and S. jonesi, and used a combination of inhibitors to determine the relative activities of P- and V-type H +-ATPases. We found that the total H +-ATPase activity of their plumes was approximately 14 μmol h −1 g −1 wet weight, and that of their roots was between 5 and 7 μmol h −1 g −1 wet weight. These activities were more than ten times lower than those measured in R. pachyptila. We suggest that seep tubeworms might use passive channels to eliminate protons across their roots, in addition to ATP-dependant proton pumps located in their plumes and roots. In addition, we found strong differences between the types of ATPase activities in the plumes of L. luymesi and S. jonesi. While the H +-ATPase activity of L. luymesi plumes is dominated by P-type ATPases, S. jonesi has an unusually high activity of V-type H +-ATPases. We suggest that S. jonesi relies on its high V-type H +-ATPase activity to drive carbon dioxide uptake across its plume surface. L. luymesi, on the other hand, might rely partially on bicarbonate uptake across its root.

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          Most cited references37

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          Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells.

          Various membrane ATPases have been tested for their sensitivity to bafilomycin A1, a macrolide antibiotic. F1F0 ATPases from bacteria and mitochondria are not affected by this antibiotic. In contrast, E1E2 ATPases--e.g., the K+-dependent (Kdp) ATPase from Escherichia coli, the Na+,K+-ATPase from ox brain, and the Ca2+-ATPase from sarcoplasmic reticulum--are moderately sensitive to this inhibitor. Finally, membrane ATPases from Neurospora vacuoles, chromaffin granules, and plant vacuoles are extremely sensitive. From this we conclude that bafilomycin A1 is a valuable tool for distinguishing among the three different types of ATPases and represents the first relatively specific potent inhibitor of vacuolar ATPases.
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            Ion motive ATPases. I. Ubiquity, properties, and significance to cell function

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              A paradox resolved: sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy.

              Vestimentiferan tubeworms, symbiotic with sulfur-oxidizing chemoautotrophic bacteria, dominate many cold-seep sites in the Gulf of Mexico. The most abundant vestimentiferan species at these sites, Lamellibrachia cf. luymesi, grows quite slowly to lengths exceeding 2 meters and lives in excess of 170-250 years. L. cf. luymesi can grow a posterior extension of its tube and tissue, termed a "root," down into sulfidic sediments below its point of original attachment. This extension can be longer than the anterior portion of the animal. Here we show, using methods optimized for detection of hydrogen sulfide down to 0.1 microM in seawater, that hydrogen sulfide was never detected around the plumes of large cold-seep vestimentiferans and rarely detectable only around the bases of mature aggregations. Respiration experiments, which exposed the root portions of L. cf. luymesi to sulfide concentrations between 51-561 microM, demonstrate that L. cf. luymesi use their roots as a respiratory surface to acquire sulfide at an average rate of 4.1 micromol x g(-1) x h(-1). Net dissolved inorganic carbon uptake across the plume of the tubeworms was shown to occur in response to exposure of the posterior (root) portion of the worms to sulfide, demonstrating that sulfide acquisition by roots of the seep vestimentiferan L. cf. luymesi can be sufficient to fuel net autotrophic total dissolved inorganic carbon uptake.
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                Author and article information

                Contributors
                +49-551-3912910 , sdattag@uni-goettingen.de
                Journal
                Mar Biol
                Mar. Biol
                Marine Biology
                Springer-Verlag (Berlin/Heidelberg )
                0025-3162
                1432-1793
                31 January 2009
                31 January 2009
                2009
                : 156
                : 779-786
                Affiliations
                [ ]Department of Biology, The Pennsylvania State University, University Park, PA 16802 USA
                [ ]Courant Research Centre Geobiology, Georg- August- Universität Göttingen, 370077 Göttingen, Germany
                Author notes

                Communicated by M. Kühl.

                Article
                1132
                10.1007/s00227-009-1132-2
                3873087
                19988573-ef11-4f6e-9d02-e444f7f83c48
                © Springer-Verlag 2009
                History
                : 21 April 2008
                : 8 January 2009
                Categories
                Original Paper
                Custom metadata
                © Springer-Verlag 2009

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