Abstract
In vivo 31P- and 13C-NMR spectra of the lugworm Arenicola marina (Polychaeta, Annelida) gathered between 1988 and 1994 at different times of the year were evaluated for seasonally dependent metabolic changes. Beside the typical 31P-NMR signals of ATP and (phospho)taurocyamine, other seasonally dependent signals were observed: from January to March an intensive signal at 1.4–1.8 ppm was identified as inorganic phosphate compartmented in an acidic intestinal lumen. Between April and September signals at 1.2–1.4 ppm were assigned to phosphodiester. Starting in July males showed a second phosphagen signal [(phospho)creatine of spermatozoa, cf. Kamp and Juretschke (1989a)] whose intensity increased until spawning in September. The (phospho)taurocyamine/ATP ratio was also dependent on the season. In January or February the ratio reached 11, while in summer and autumn the ratio was between 4 and 5. As verified by biochemical assays this effect was caused by a significant decrease of ATP in the lugworm body wall during winter (December–February). The phosphagen (phospho)taurocyamine and the respective unphosphorylated guanidine taurocyamine remained constant throughout the year. Levels of free inorganic phosphate incurred similar changes to ATP. 13C-NMR spectra of lugworms showed a dramatic change in lipid stores. They were below the detection limit between January and March but developed into the most intensive signals during summer. The most abundant amino acids, glycine and alanine, were observed throughout the year while glycogen could not be detected in the 13C-NMR spectra. After treating tissue extracts with amyloglucosidase, the signals of the hydrolytic product glucose were recorded indicative of NMR-invisible glycogen stores.
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Abbreviations
- AN :
-
adenine nucleotides
- NMR :
-
nuclear magnetic resonance
- P i :
-
inorganic phosphate
- (P)Cr :
-
(phospho)creatine
- PDE :
-
phosphodiester
- PME :
-
phosphomonoester
- PPA :
-
phenylphosphonic acid
- (P)Tc :
-
(phospho)taurocyamine
References
Bentley MG, Pacey AA (1989) A scanning electron microscopical study of sperm development and activation in Arenicola marina L. (Annelida: Polychaeta). Invertebr Reprod Dev 15: 211–219
Bergmeyer HU (1984/85) Methods of enzymatic analysis vol. VI/VII and VIII. Verlag Chemie, Weinheim
Borgs M, Hecke P van, Overloop K, Decanniere C, Huffel S van, Stalmans W, Vanstapel F (1993) In situ 13C-NMR quantification of hepatic glycogen. NMR in Biomed 6: 371–376
Bury NR, Olive PJW (1993) Ultrastructural observations on membrane changes associated with cryopreserved spermatozoa of two polychaete species and subsequent mobility induced by quinacine. Invertebr Reprod Dev 23: 139–150
Canioni P, Alger JR, Shulman RG (1983) Natural abundance carbon-13 nuclear magnetic resonance spectroscopy of liver and adipose tissue of the living rat. Biochemistry 22: 4974–4980
Cerdan S, Seelig J (1990) NMR studies of metabolism. Annu Rev Biophys Chem 19: 43–67
Eberhardt J (1982) Untersuchungen über den Einfluß der jahreszeit und von Hunger auf den Stoffwechsel des Wattwurmes Arenicola marina. Diplomarboit, Universität Münster
Eberhardt J (1988) pH-Wert-Änderungen im Darmlumen von Arenicola marina (Polychaeta) und ihre mögliche physiologische Bedeutung. Verh Dtsch Zool Ges 81: 308
Eberhardt J (1992) Isolation and characterization of five serine proteases with trypsin-, chymotrypsin- and elastase-like characteristics from the gut of the lugworm Arenicola marina (Polychaeta). J Comp Physiol B 162: 159–167
Gabbott PA (1980) Seasonal changes in the specific activities of the pentose phosphate cycle enzymes, G6PDH and 6PGDH, and NADP-dependent isocitrate dehydrogenase in the bivalves Mytilus edulis, Ostrea edulis and Crassostrea gigas. Comp Biochem Physiol 66B: 279–284
Gabbott PA (1983) Development and seasonal metabolic activities in marine molluses. In: Wilbur KM, Hochachka PW (eds) The mollusca, environmental biochemistry and physiology, vol 2. Academic Press, New York, pp 165–218
Grieshaber M (1992) Hypoxia and sulfide tolerance in some marine invertebrates. Verh Dtsch Zool Ges 85: 55–76
Griffiths JR (1981) A fresh look at glycogenolysis in skeletal muscle. Biosci Rep 1: 595–610
Hazel JR, Prosser CL (1974) Molecular mechanisms of temperature compensation in poikilotherms. Physiol Rev 54: 620–677
Hochachka PW, Somero GN (1973) Strategies of biochemical adaptation. Saunders, Philadelphia
Howie DID (1984) The reproductive biology of the lugworm, Arenicola marina L.. In: Fischer A, Pfannenstiel HD (eds) Polychaete Reproduction, Fortschritte der Zoologie, Vol 29. Fischer Stuttgart, pp 247–263
Hoffmann KH (1983) Metabolic and enzyme adaptation to temperature and pressure. In: Wilbur KM, Hochachka PW (eds) The Mollusca, environmental biochemistry and physiology, vol 2. Academic Press, New York, pp 219–255
Hull WE, Zerfowski M, Bannasch P (1987) Quantification of glycogen in tissue by means of 13C-NMR: application to human kidney tumors. Sixth Annual Meeting and Exhibition of the Society of Magnetic Resonance in Medicine, vol 1. p 488
Juretschke HP, Kamp G (1990a) Influence of intracellular pH on reduction of energy metabolism during hypoxia in the lugworm Arenicola marina. J Exp Zool 256, 255–263
Juretschke HP, Kamp G (1990b) In vivo 13C-NMR studies on the metabolism of the lugworm Arenicola marina. Eur J Biochem 193: 273–281
Kamp G, Juretschke HP (1987) An in vivo 31P-NMR study of the possible regulation of glycogen phosphorylase a by phosphagen via phosphate in the abdominal muscle of the shrimp Crangon crangon. Biochim Biophys Acta 929: 121–127
Kamp G, Juretschke HP (1989a) Phosphagen heterogeneity during reproductive cycle in the lugworm Arenicola marina. Naturwissenschaften 76: 275–276
Kamp G, Juretschke HP (1989b) Hypercapnic and hypocapnic hypoxia in the lugworm Arenicola marina: a 31P-NMR study. J Exp Zool 252: 219–227
Kamp G (1993) Intracellular reactions controlling environmental anacrobiosis in the marine annelid Arenicola marina, A fresh look at old pathways. In: Hochachka PW et al. (eds) Surviving hypoxia. CRC Press, Boca Raton, pp 5–17
Kamp G, Juretschke HP, Thiel U, Englisch H (1995) In vivo nuclear magnetic resonance on the lugworm Arenicola marina. I Free inorganic phosphate and free adenylmonophosphate concentrations in the body wall and their dependence on hypoxia. J Comp Physiol 165: 143–152
Kawano Y, Tanokura M, Yamada K (1988) Phosphorus nuclear magnetic resonance studies on the effect of duration of contraction in bull-frog skeletal muscles. J Physiol (London) 407: 243–261
Kushmerick MJ, Meyer RA, Brown TR (1992) Regulation of oxygen consumption in fast- and slow-twitch muscle. Am J Physiol 263: C598-C606
Newell RC, Branch GM (1980) The influence of temperature on the maintenance of metabolic energy balance in marine invertebrates. In: Blaxter et al. (eds) Advances in marine biology, vol 17. Academic Press, New York
Norton RS (1979) Identification of mollusc metabolites by naturalabundance 13C-NMR studies of whole tissue and tissue homogenates. Comp Biochem Physiol 63B: 67–72
Overloop K, Steegmans A, Waebens M, Hecke P van, Vanstapel F, Stalmans W (1991) In-vitro NMR visibility of the 13C-1 of the glucosyl residues in hepatic glycogen. Annual Meeting and Exhibition of the Society of Magnetic Resonance in Medicine, p 1194
Pörtner HO, Surholt B, Grieshaber M (1979) Recovery from anaerobiosis of the lugworm, Arenicola marina L.: changes of metabolite concentrations in the body wall musculatures. J Comp Physiol 133: 227–231
Reitze M, Schöttler U (1989) The time dependence of adaptation to reduced salinity in the lugworm Arenicola marina L. (Annelida: Polychaeta). Comp Biochem Physiol 93A: 549–559
Reitze M, Schöttler U, Luftmann H (1989) Alanine metabolism of the lugworm Arenicola marina L. (Annelida: Polychaeta) during adaptation to reduced salinity. Comp Biochem Physiol 93B: 689–696
Schöttler U (1989) Anaerobic metabolism in the lugworm Arenicola marina during low tide: the influence of developing reproductive cells. Comp Biochem Physiol 92A 1–7
Schöttler U, Bennet EM (1991) Annelids. In: Bryant C Bury (ed) Metazoan life without oxygen. St. Edmundsbury Press, St. Edmunds, pp 165–185
Siegmund B, Grieshaber M, Reitze M, Zebe E (1985) Alanopine and strombine are end products of anaerobic glycolysis in the lugworm Arenicola marina L. (Annelida, Polychaeta). Comp Biochem Physiol 82B: 337–345
Taylor DJ, Styles P, Matthews PM, Arnold DA, Gadian DG, Bore P, Radda GK (1986) Energetics of human muscle: exercise-induced ATP depletion. Magn Reson Med 3: 44–54
Vanstapel F, Waebens M, Hecke P van, Decanniere C, Stalmans W (1990) The cytosolic concentration of phosphate determines the maximal rate of glycogenolysis in perfused rat liver. Biochem J 266: 207–212
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Communicated by H. Langer
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Juretschke, H.P., Kamp, G. In vivo nuclear magnetic resonance studies on the lugworm Arenicola marina. II Seasonal changes of metabolism. J Comp Physiol B 165, 153–160 (1995). https://doi.org/10.1007/BF00301479
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DOI: https://doi.org/10.1007/BF00301479