Abstract
This study concerns the effects of oxygen deprivation due to incubation in oxygen free sea water (environmental anoxia) or exercise (functional anoxia) and of exposure to air on the mode of energy production in the foot of the whelk Nassa mutabilis. Additionally, energy metabolism of the foot muscle was investigated during exercise after different anoxia periods and during the subsequent recovery period. During environmental anoxia, phosphoarginine, glycogen and aspartate are broken down as substrates and alanine and succinate are formed as products. There was no production of D-lactate or octopine. The energy charge value fell after 24-h anoxia. Exposure to air resulted in only small changes in phosphoarginine and alanine levels, suggesting that oxygen uptake was impaired in the first phase of air exposure but that, later, aerial respiration kept pace with the energy demand. Exercise caused a dramatic decrease of phosphoarginine concentration, coupled with glycolytic ATP production via octopine formation. In the recovery period (after exercise), the level of phosphoarginine was rapidly restored. An anaerobic component was evident during recovery as shown by the accumulation of D-lactate. Thus, both terminal dehydrogenases, octopine- and lactate dehydrogenase, are active in the muscle, but under different physiological conditions. Octopine formation also took place when the whelks were subjected to exercise after 4 or 24 h of anoxia. In this case, glycolysis provided between 70 and 90% of the energy required since the phosphagen store had already been depleted during the anoxic period. When the work load was increased (greater number of leaps), it became evident that the action of arginine kinase and octopine dehydrogenase are not closely linked. First there was an increase of arginine and then later a condensation of arginine with pyruvate to form octopine.
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Baldwin, J., A. K. Lee and W. R. England: The functions of octopine dehydrogenase and D-lactate dehydrogenase in the pedal retraotor muscle of the dog whelk Nassarius coronatus (Gastropoda: Nassariidae). Mar. Biol. 62, 235–238 (1981)
Bauer, V.: Notizen aus einem biologischen Laboratorium am Mittelmeer. Int. Rev. Hydrob. 6, 31–37 (1913)
Bergmeyer, H. U., E. Bernt, H. Möllering and G. Pfleiderer: L-Aspartat and L-Asparagin. In: Methoden der enzymatischen Analyse, Vol 2, pp 1741–1745. Ed. by H. U. Bergmeyer. 3rd ed. Weinheim: Verlag Chemie 1974
Brand, T. von, H. D. Baernstein and B. Mehlman: Studies on the anaerobic metabolism and the aerobic carbohydrate consumption of some fresh water snails. Biol. Bull. mar. biol. Lab., Woods Hole 98, 266–276 (1950)
Carlsson, K. H. and G. Gäde: Anaerobic metabolism of the horseshoe crab, Limulus polyphemus: tissue-specific isoenzymes of D-specific lactate dehydrogenase and lactate metabolism. In: Exogenous and endogenous influences on metabolic and neural control, Vol. 2, p 128. Ed. by A. D. F. Addink and N. Spronk. Oxford: Pergamon Press 1982
Carlsson, K. H. and G. Gäde: L-Alanin als wichtiges Endprodukt bei biotopbedingter Anaerobiose von Limulus polyphemus. Verh. dtsch. Zool. Ges. Bonn, p 274 (1983)
Chih, C. P. and W. R. Ellington: Energy metabolism during contractile activity and environmental hypoxia in the phasic adductor muscle of the bay scallop Argopecten irradians concentricus. Physiol. Zool. 56, 623–631 (1983)
Ellington, W. R.: Energy metabolism during hypoxia in the isolated perfused ventricle of the Whelk, Busycon contrarium Conrad. J. comp. Physiol. 142, 457–464 (1981)
Ellington, W. R.: Metabolism at the pyruvate branch point in the radula retractor muscle of the whelk, Busycon contrarium. Can. J. Zool. 60, 2973–2977 (1982)
Gäde, G.: Biological role of octopine formation in marine molluscs. Mar. Biol. Lett. 1, 121–135 (1980a)
Gäde, G.: The energy metabolism of the foot muscle of the jumping cockle, Cardium tuberculatum: sustained anoxia versus muscular activity. J. comp. Physiol. 137, 177–182 (1980b)
Gäde, G.: Energy production during swimming in the adductor muscle of the bivalve Lima hians: comparison with the data from other bivalve mollusks. Physiol. Zool. 54, 400–406 (1981)
Gäde, G.: Energy metabolism of arthropods and mollusks during environmental and functional anaerobiosis. J. exp. Zool. 228, 415–429 (1983)
Gäde, G. and M. Grieshaber: A rapid and specific enzymatic method for the estimation of L-arginine. Anal. Biochem. 66, 393–399 (1975)
Gäde, G. and E.J.H. Head: A rapid method for the purification of octopine dehydrogenase for the determination of cell metabolites. Experientia 35, 304–305 (1979)
Gäde, G., E. Weeda and P. A. Gabbott: Changes in the level of octopine during the escape responses of the scallop. Pecten maximus (L.). J. comp. Physiol. 124, 121–127 (1978)
Gäde, G., H. Wilps, J. H. F. M. Kluytmans and A. de Zwaan: Glycogen degradation and end products of anaerobic metabolism in the fresh water bivalve Anodonta cygnea. J. comp. Physiol. 104, 79–85 (1975)
Gawehn, K. and H. U. Bergmeyer: D-Lactat. In: Methoden der enzymatischen Analyse, Vol. 2, pp 1538–1541. Ed. by H. U. Bergmeyer. Weinheim: Verlag Chemie 1974
Grieshaber, M.: Breakdown and formation of high-energy phosphates and octopine in the adductor muscle of the scallop, Chlamys opercularis (L.), during escape swimming and recovery. J. comp. Physiol. 126, 269–276 (1978)
Grieshaber, M., E. Kronig and R. Koormann: A photometric estimation of phospho-L-arginine, arginine and octopine using homogenous octopine dehydrogenase isoenzyme 2 from the squid, Loligo vulgaris. Hoppe Seylers Z. Physiol. Chem. 359, 133–136 (1978)
Hoffmann, H.: Über den Fluchtreflex bei Nassa. Zool. Anz. 4 (Suppl.), Verh. Dtsch. Zool. Ges. (Marburg), 112–118 (1929)
Jaworeck, D., W. Gruber and H. U. Bergmeyer: Adenosin-5′-diphosphat und Adenosin-5′-monophosphat. In: Methoden der enzymatischen Analyse, Vol. 2, pp 2179–2181. Ed. by H. U. Bergmeyer, 3rd ed. Weinheim: Verlag Chemie 1974
Kluytmans, J. H., P. R. Veenhof and A. de Zwaan: Anaerobic production of volatile fatty acids in the sea mussel Mytilus edulis L. J. comp. Physiol. 104, 71–78 (1975)
Koormann, R. and M. Grieshaber: Investigations on the energy metabolism and on octopine formation of the common whelk, Buccinum undatum L., during escape and recovery. Comp. Biochem. Physiol. 65 B, 543–547 (1980)
Kushins, L. J. and C. P. Mangum: Responses to low oxygen conditions in two species of the mud snail Nassarius. Comp. Biochem. Physiol. 39 A, 421–435 (1971)
Lamprecht, W. and I. Trautschold: ATP; Bestimmung mit Hexokinase und Glucose-6-phosphat-Dehydrogenase. In: Methoden der enzymatischen Analyse, Vol. 2, pp 2151–2159. Ed. by H. U. Bergmeyer, 3rd ed. Weinheim: Verlag Chemie 1974
Livingstone, D. R.: Energy production in the muscles of different kinds of molluscs. In: Exogenous and endogenous influences on metabolic and neural control, Vol. 1, pp 257–274. Ed. by A. D. F. Addink and N. Spronk. Oxford: Pergamon Press 1982
Meinardus, G. and G. Gäde: Zur physiologischen Bedeutung der drei terminalen Dehydrogenasen der Glykolyse bei der Herzmuschel Cardium tuberculatum. Verh. dtsch. Zool. Ges. Bonn p 307 (1983)
Weber, H.: Ein Umdreh- und ein Fluchtreflex bei Nassa mutabilis. Zool. Anz. 60, 261–269 (1924)
Weber, H.: Über die Umdrehreflexe einiger Prosobranchier des Golfes von Neapel. Z. vergl. Physiol. 3, 389–474 (1926)
Wieser, W.: The initial stage of anaerobic metabolism in the snail, Helix pomatia. FEBS Lett. 95, 375–378 (1978)
Wieser, W.: Metabolic end products in three species of marine gastropods. J. mar. biol. Assoc. U.K. 80, 175–180 (1980)
Williamson, D. H.: L-Alanin. Bestimmung mit Alanin-Dehydrogenase. In: Methoden der enzymatischen Analyse, Vol. 2, pp 1724–1727. Ed. by H. U. Bergmeyer, 3rd ed. Weinheim: Verlag Chemie 1974
Williamson, J. R.: Succinat. In: Methoden der enzymatischen Analyse, Vol. 2, pp 1661–1666. Ed. by H. U. Bergmeyer, 3rd ed. Weinheim: Verlag Chemie 1974
Zwaan, A. de: Carbohydrate metabolism in bivalves. In: The mollusca, Vol. 1, Metabolic biochemistry and molecular biomechanics, pp 137–175. Ed. by P. W. Hochachka. New York: Academic Press 1983
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Communicated by O. Kinne, Hamburg
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Gäde, G., Carlsson, K.H. & Meinardus, G. Energy metabolism in the foot of the marine gastropod Nassa mutabilis during environmental and functional anaerobiosis. Marine Biology 80, 49–56 (1984). https://doi.org/10.1007/BF00393127
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DOI: https://doi.org/10.1007/BF00393127