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Metabolic compensation to reduced oxygen tensions in the sea cucumber,Sclerodactyla briareus (Leseur)

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Summary

Carbohydrate metabolism of the sea cucumber,Sclerodactyla briareus, was investigated in an effort to find metabolic pathways that might be useful during exposure to hypoxic conditions. The utilization of glucose-U-14C by in vitro longitudinal muscle preparations was not enhanced during exposure to reduced oxygen tensions. Alanine was the most highly labelled compound regardless of incubation conditions. Hypoxic exposure resulted in a four-fold increase in radioactivity in lactate, and decreased radioactivity in alanine, glutamate and aspartate. Succinate and volatile acids were not observed to be significant end products of anaerobic glycolysis inS. briareus longitudinal muscle. The relative activities of a number of glycolytic and gluconeogenic enzymes in longitudinal muscle were consistent with the observations of isotope distribution. Levels of lactate in muscle tissue of sea cucumbers exposed to 24 and 48 h of hypoxia were on the average 20 times higher than the values for aerobic controls. The kinetic characteristics of longitudinal muscle lactate dehydrogenase coupled with hypoxic acid release and the lack of an oxygen debt phenomenon by in vitro longitudinal muscle preparations indicate that lactate may not be appreciably oxidized in this tissue but is released into the body fluids. Unlike many anoxia-tolerant invertebrates which produce primarily succinate during exposure to reduced oxygen tensions, specimens ofSclerodactyla briareus produce lactate as a major glycolytic end product.

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Abbreviations

AAT:

alanine aminotransferase

ADP:

adenosine-5′-diphosphate

DHAP:

dihydroxyacetone phosphate

IDP:

inosine-5′-diphosphate

LDH:

lactate dehydrogenase

MDH:

malate dehydrogenase

NAD:

nicotinamide adenine dinucleotide

NADP:

nicotinamide adenine dinucleotide phosphate

PEPCK:

phosphoenolpyruvate carboxykinase

PK:

pyruvate kinase

References

  • Barker, S.B., Summerson, W.H.: The colorimetric determination of lactic acid in biological material. J. biol. Chem.138, 534–554 (1941)

    Google Scholar 

  • Barnes, H., Finlayson, D.M., Piatigorsky, J.: The effect of desiccation and anaerobic conditions on the behavior, survival and general metabolism of three common cirrepedes. J. Anim. Ecol.32, 233–252 (1963)

    Google Scholar 

  • Boyland, E.: Chemical changes in muscle. II. Invertebrate muscle. Biochem. J.22, 362–376 (1928)

    Google Scholar 

  • Brand, T. v., Baernstein, H.D., Mehlman, B.: Studies on the anaerobic metabolism and the aerobic carbohydrate content of some fresh water snails. Biol. Bull.98, 266–276 (1950)

    Google Scholar 

  • Buddington, R.A.: The normal spontaneity of movement of the respiratory muscles ofThyone briareus Leseur. Physiol. Zool.10, 141–155 (1937)

    Google Scholar 

  • Chen, C., Awapara, J.: Intracellular distribution of enzymes catalyzing succinate production from glucose inRangia mantle. Comp. Biochem. Physiol.30, 727–737 (1969a)

    Google Scholar 

  • Chen, C., Awapara, J.: Effect of oxygen on the end products of glycolysis inRangia cuneata. Comp. Biochem. Physiol.31, 395–401 (1969b)

    Google Scholar 

  • Cleland, K.W., Lord Rothschild: The metabolism of the sea urchin egg. Anaerobic breakdown of carbohydrate. J. exp. Biol.29, 285–294 (1952)

    Google Scholar 

  • Dales, R.P.: Survival of anaerobic periods by two intertidal polychaetesArenicola marina andOwenia fusiformis Delle Chiaje. J. mar. biol. Assoc. U.K.37, 521–529 (1958)

    Google Scholar 

  • Dubois, M., Gilles, K.A., Ng, Y.C., Nichols, A.V.: Colorimetric method for the determination of sugars and related substances. Analyt. Chem.28, 350–356 (1956)

    Google Scholar 

  • Dunnington, E.A.: Survival time of oysters after burial at various temperatures. Proc. Nat. Shellfish Assoc.58, 101–103 (1968)

    Google Scholar 

  • Ellington, W.R.: Holothurian facultative anaerobiosis. Amer. Zool.15, 808 (1975)

    Google Scholar 

  • Ellington, W.R.: L-Lactate dehydrogenase in the longitudinal muscle of the sea cucumber,Sclerodactyla briareus (Echinodermata: Holothuroidea). Mar. Biol.36, 31–36 (1976)

    Google Scholar 

  • Gäde, G.: Anaerobic metabolism in the common cockle,Cardium edule. I. The utilization of glycogen and accumulation of multiple end products. Arch. Int. Physiol. Biochem.83, 879–886 (1975)

    Google Scholar 

  • Gäde, G., Wilps, H.: Glycogen degradation and end products of anaerobic metabolism in the freshwater bivalveAnodonta cygnea. J. comp. Physiol.104, 74–85 (1975)

    Google Scholar 

  • Garber, A.J., Karl, I.E., Kipnis, D.M.: Alanine and glutamine synthesis and release from skeletal muscle. J. biol. Chem.251, 826–835 (1976)

    Google Scholar 

  • Gay, W.S., Simon, S.E.: Metabolic control in holothuroidean muscle. Comp. Biochem. Physiol.11, 183–192 (1964)

    Google Scholar 

  • Goforth, H.W.: Metabolic end products of the American oyster,Crassostrea virginica (Gmelin). M.A. Thesis, University of South Florida, Tampa 1974

    Google Scholar 

  • Hammen, C.S.: Metabolism of the oyster,Crassostrea virginica. Amer. Zool.9, 309–318 (1969)

    Google Scholar 

  • Hammen, C.S.: Respiratory adaptations: Invertebrates. Proc. Third Int. Estuarine Res. Symp. (ed. M.L. Wiley) New York: Academic Press 1977

    Google Scholar 

  • Hammen, C.S., Osborne, B.J.: Carbon dioxide fixation in marine invertebrates: A survey of major phyla. Science130:1409–1410 (1959)

    Google Scholar 

  • Hochachka, P.W., Fields, J., Mustafa, T.: Animal life without oxygen: Basic biochemical mechanisms. Amer. Zool.13, 543–555 (1973)

    Google Scholar 

  • Hochachka, P.W., Storey, K.B.: Metabolic consequences of diving in animals and man. Science187, 613–621 (1975)

    Google Scholar 

  • Hohorst, H.J., Arese, P., Bartels, H., Stratman, D., Talke, H.: L(+) Lactic acid and the steady state of cellular RED/OX systems. Ann. N.Y. Acad. Sci.119, 974–994 (1965)

    Google Scholar 

  • Kluytmans, J.H., Veenhof, P.R., de Zwaan, A.: Anaerobic production of volatile fatty acids in the sea musselMytilus edulis L. J. comp. Physiol.104, 71–78 (1975)

    Google Scholar 

  • Mangum, C.P.: Evaluation of the functional properties of invertebrate hemoglobins. Neth. J. Sea Res.7, 303–315 (1973)

    Google Scholar 

  • Mangum, C.P., van Winkle, W.: Responses of aquatic invertebrates to declining oxygen tensions. Amer. Zool.13, 529–541 (1973)

    Google Scholar 

  • McManus, D.P., James, B.L.: Anaerobic glucose metabolism in the digestive gland ofLittorina saxatilis rudis (Maton) and in the daughter sporocysts ofMicrophallus similis (Jäg) (Digenea: Microphallidae). Comp. Biochem. Physiol.51B, 293–297 (1975)

    Google Scholar 

  • Mehlman, B., Brand, T. v.: Further studies on the anaerobic metabolism of some fresh water snails. Biol. Bull.100, 199–205 (1951)

    Google Scholar 

  • Monroy, A., Vittorelli, M.L.: Utilization of14C-glucose for amino acid and protein synthesis by the sea urchin embryo. J. cell. comp. Physiol.60, 285–287 (1962)

    Google Scholar 

  • Odessey, R., Khairallah, E.A., Goldberg, A.L.: Origin and possible significance of alanine production by skeletal muscle. J. biol. Chem.249, 7623–7629 (1974)

    Google Scholar 

  • Sassaman, C., Mangum, C.P.: Relationship between aerobic and anaerobic metabolism in estuarine anemones. Comp. Biochem. Physiol.44A, 1313–1319 (1973)

    Google Scholar 

  • Stokes, T.M., Awapara, J.: Alanine and succinate as end products of glucose degradation in the clam,Rangia cuneata. Comp. Biochem. Physiol.25, 883–882 (1968)

    Google Scholar 

  • Theede, H.: Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on bottom marine invertebrates. Neth. J. Sea Res.7, 244–252 (1973)

    Google Scholar 

  • Williamson, D.H., Lopes-Vieira, O., Walker, B.: Concentratioms of free glucogenic amino acids in livers of rats subjected to various metabolic stresses. Biochem. J.104, 497–502 (1967)

    Google Scholar 

  • Zebe, E.: In vivo Untersuchungen über die Glucose-Abbau beiArenicola marina (Annelida, Polychaeta). J. comp. Physiol.101, 133–145 (1975)

    Google Scholar 

  • Zwaan, A. de, Bont, A.M.T. de, Kluytmans, J.H.: Metabolic adaptations on the aerobic-anaerobic transition in the sea musselMytilus edulis (L). Proc. 9th Europ. mar. biol. Symp. 121–138 (1975)

  • Zwaan, A. de, Zandee, D.I.: The utilization of glycogen and accumulation of some intermediates during anaerobiosis inMytilus edulis L. Comp. Biochem. Physiol.43B, 47–54 (1972)

    Google Scholar 

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Author notes

  1. W. Ross Ellington

    Present address: Seaver Chemistry Laboratory, Pomona College, 91711, Claremont, California, USA

Authors and Affiliations

  1. Department of Zoology, University of Rhode Island, 02881, Kingston, Rhode Island, USA

    W. Ross Ellington & C. S. Hammen

Authors
  1. W. Ross Ellington
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  2. C. S. Hammen
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Additional information

A brief account of some of this work was published inAmerican Zoologist 15, 808 (1975). This work is derived from portions of a dissertation submitted to the University of Rhode Island by the senior author in partial fulfillment of the degree of Doctor of Philosophy. Partial support of this research was provided by a Society of the Sigma Xi Grant-in-Aid for Research

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Ross Ellington, W., Hammen, C.S. Metabolic compensation to reduced oxygen tensions in the sea cucumber,Sclerodactyla briareus (Leseur). J Comp Physiol B 122, 347–358 (1977). https://doi.org/10.1007/BF00692520

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  • DOI: https://doi.org/10.1007/BF00692520

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