Abstract
Specimens of the hydrothermal vent pogonophoran Riftia pachyptila Jones were collected by submersible at a depth of 2 600 m at the 21°N hydrothermal vent site on the East Pacific Rise (20°50′N, 109°06′W) in April and May of 1982. The worms were maintained in pressurized aquaria for up to 45 d for metabolic studies. Consumption of O2 was regulated down to low PO 2 (oxygen partial pressure) values; O2 consumption rates were 0.63 and 1.12 μ mol g-1 wet wt h-1 at 2.5° and 8°C, respectively; such rates were comparable to those previously measured for other pogonophorans. Intact specimens of R. pachyptila (including bacterial symbionts) did not consume significant amounts of CH4 from the environment. The respiratory quotients, in the absence of added sulfide, indicated that metabolism was mainly heterotrophic. High rates of uptake of dissolved amino acids were recorded for one specimen. The total [CO2] in the vascular blood and the Hb-containing coelomic fluid were high. Under anaerobic conditions, there were equilibrium distributions of pH, total [CO2] and sulfide concentrations between the vascular blood and the coelomic fluid, apparently because these metabolites were readily exchanged between the two compartments. The vascular blood bound neither CH4 nor H2. However, sulfide was reversibly bound by both the vascular blood and coelomic fluid; because this binding depended strongly on pH (with a maximum at about 7.5), HS- was probably the molecular species bound. Under anaerobic, but not aerobic conditions, the trophosome bound substantial amount of sulfide; thus, the high concentrations of sulfide in the trophosome may have resulted mainly from sulfide bound to sulfide oxidases under anaerobic conditions. The coelomic fluid had a relatively low buffering capacity (2.2 mmol CO2ΔpH-1).
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Literature cited
Arp, A. J. and J. J. Childress: Blood function in the hydrothermal vent vestimentiferan tube worm. Science, N.Y., 213, 342–344 (1981a)
Arp, A. J. and J. J. Childress: Functional characteristics of the blood of the deep-sea hydrothermal vent brachyuran crab. Science, N.Y. 214, 559–561 (1981b)
Arp, A. J. and J. J. Childress: Sulfide binding by the blood of the hydrothermal vent tube worm Riftia pachyptila. Science, N.Y. 219, 295–297 (1983)
Bezkorovainy, A.: Biochemistry of nonheme iron, 435 pp. New York: Plenum Press 1980
Cavanaugh, C. M., S. L. Gardiner, M. L. Jones, H. W. Jannasch and J. B. Waterbury: Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science, N.Y. 213, 340–342 (1981)
Childress, J. J. and T. J. Mickel: A motion compensated shipboard precision balance system. Deep-Sea Res. 27A, 965–970 (1980)
Childress, J. J. and T. J. Mickel: Oxygen and sulfide consumption rates of the vent clam Calyptogena pacifica. Mar. Biol. Lett. 3, 73–79 (1982)
Felbeck, H.: Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science, N.Y. 213, 336–338 (1981)
Felbeck, H. and G. N. Somero: Primary production in deep-sea hydrothermal vent organisms: roles of sulfide oxidizing bacteria. Trends Biochem. Sci. 7, 201–204 (1982)
Fisher, C. R., Jr. and J. J. Childress: Substrate oxidation by trophosome tissue from Riftia pachyptila Jones (phylum Pogonophora). Mar. Biol. Lett. 5, 171–183 (1984)
Hand, S. C. and G. N. Somero: Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment. Biol. Bull. mar. biol. Lab., Woods Hole 165, 167–181 (1983)
Hessler, R. R. and W. Smithey: The distribution and community structure of megafauna at the Galapagos rift hydrothermal vents. NATO Conf. Ser. (mar. Sciences) 12, 735–770 (1984)
Ivanov, A. V.: Pogonophora, 479 pp. New York: Consultants Bureau 1963
Jannasch, H. W.: Microbial processes at deep sea hydrothermal vents. NATO Conf. Ser. (mar. Sciences) 12, 677–709 (1984)
Jones, M. L.: Riftia pachyptila, new genus, new species, the vestimentiferan worm from the Galápagos rift geothermal vents (Pogonophora). Proc. biol. Soc. Wash. 93, 1295–1313 (1981)
Krüger, F.: Versuche über die Abhängigkeit der Atmung von Arenicola marina (Annelides Polychaeta) von Größe und Temperatur. Helgoländer wiss. Meeresunters. 10, 38–63 (1964)
Lapennas, G. N., J. M. Colacino and J. Bonaventura: Thin-layer methods for determination of oxygen binding curves of hemoglobin solutions and red blood cells. In: Methods in enzymology, Vol. 76. pp 449–470. Ed. by E. Antonini, L. Rossi-Bernardi and E. Chianco. New York: Academic Press 1981
Lindroth, P. and K. Mopper: High performance liquid chromatographic determination of subpicomole amounts of amino acids by precolumn fluorescence derivitization with o-phthaldialdehyde. Analyt. Chem. 51, 1667–1674 (1979)
Little, C. and B. Gupta: Studies on Pogonophora. III. Uptake of nutrients. J. exp. Biol. 51, 759–793 (1969)
Mangum, C. P.: Evaluation of the functional properties of invertebrate hemoglobins. Neth. J. Sea Res. 7, 303–315 (1973)
Mangum, C. P.: The oxygenation of hemoglobin in lugworms. Physiol. Zoöl. 49, 85–99 (1976)
Manwell, C., E. C. Southward and A. J. Southward: Preliminary studies on haemoglobin and other proteins of the Pogonophora. J. mar. biol. Ass. U.K. 46, 115–124 (1966)
McIlvaine, T. C.: A buffer solution for colorimetric comparison. J. biol. Chem. 49, 183–186 (1921)
Mickel, T. J. and J. J. Childress: Effects of temperature, pressure and oxygen concentration on the oxygen consumption rate of the hydrothermal vent crabs Bythograea thermydron (Brachyura). Physiol. Zoöl. 55, 199–207 (1982)
Powell, M. A. and G. N. Somero: Blood components prevent sulfide poisoning of respiration of the hydrothermal vent tube worm Riftia pachyptila. Science, N.Y. 219, 297–299 (1983)
Quentin, L. B. and J. J. Childress: Observations on the swimming activity of two bathypelagic mysid species maintained at high hydrostatic pressures. Deep-Sea Res. 27A, 383–391 (1980)
Rau, G. H.: Low 15N/14N in hydrothermal vent animals: ecological implications. Nature, Lond. 289, 484–485 (1981a)
Rau, G. H.: Hydrothermal vent clam and tube worm 13C/12C: futher evidence of nonphotosynthetic food sources. Science, N.Y. 209, 338–339 (1981b)
Sober, H. A.: Handbook of biochemistry, 1622 pp. Cleveland, Ohio: The Chemical Rubber Co. 1970
Southward, A. J. and E. C. Southward: The role of dissolved organic matter in the nutrition of deep-sea benthos. Am. Zool. 22, 647–659 (1982)
Southward, A. J. and E. C. Southward, P. R. Dando, G. H. Rau, H. Felbeck and H. Flugel: Bacterial symbionts and low 13C/12C ratios in tissues of Pogonophora indicate unusual nutrition and metabolism. Nature, Lond. 293, 616–620 (1981)
Southward, E. C.: Bacterial symbionts in Pogonophora. J. mar. biol. Ass. U.K. 62, 889–906 (1982)
Stephens, G. C.: Recent progress in the study of “Die Ernährung der Wassertiere und der Stoffhaushalt der Gewässer. Am. Zool. 22, 611–619 (1982)
Terwilliger, R. C., N. B. Terwilliger and E. Schabtach: The structure of hemoglobin from an unusual deep-sea worm (Vestimentifera). Comp. Biochem. Physiol. 65B, 531–535 (1980)
Toulmond, A.: Tide-related changes of blood respiratory variables in the lugworm Arenicola marina (L.). Respir. Physiol. 19, 130–144 (1973)
Wells, R. M. G. and N. W. Pankhurst: An investigation into the formation of sulphide and oxidation compounds from the haemoglobin of the lugworm Abarenicola affinis (Ashworth). Comp. Biochem. Physiol. 66C, 255–259 (1980)
Wells, R. M. G. and L. M. Warren: The function of the cellular haemoglobins in Capitella capitata (Fabricius) and Notomastus latericeus Sars (Capitellidae: Polychaeta). Comp. Biochem. Physiol. 51A, 737–740 (1975)
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Communicated by N. D. Holland, La Jolla
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Childress, J.J., Arp, A.J. & Fisher, C.R. Metabolic and blood characteristics of the hydrothermal vent tube-worm Riftia pachyptila . Mar. Biol. 83, 109–124 (1984). https://doi.org/10.1007/BF00394718
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DOI: https://doi.org/10.1007/BF00394718