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Effectors of metabolic depression in an estivating pulmonate snail (Helix aspersa): whole animal and in vitro tissue studies

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Abstract

We have examined metabolic depression in the land snail (Helix aspersa) during estivation, and have developed a tissue model of metabolic depression using an in vitro mantle preparation. The metabolic rate ofH. aspersa is depressed by 84% in vivo within 4 weeks of onset of estivation, and this metabolic depression is accompanied by a decrease in haemolymphPO2 and pH, and an increase in haemolymphPCO2. The in vitro mantle preparation has a stable O2 consumption and energy charge, and an energy charge similar to that of mantle in vivo. The in vitro mantle is an O2-conforming tissue, withVO2 varying curvilinearly withPO2. Consequently, we have developed a mathematical method of calculating tissueVO2 at anyPO2. These calculations show that under appropriate incubation conditions of pH andPO2, the mantle from estivating animals shows a stable in vitro metabolic depression of 48% compared to mantle from control snails. The extrinsic effects ofPO2 and pH account for 70% of the total in vitro metabolic depression of mantle tissue; intrinsic effectors contribute a further 30%.

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Abbreviations

BMS :

blood micro system

MD :

inetabolic depression

MR :

metabolic rate

[O 2]:

concentration of oxygen

PCO 2 :

partial pressure of carbon dioxide

PO 2 :

partial pressure of oxygen

SE :

standard error

STP :

standard temperature and pressure

VO 2 :

rate of oxygen consumption

References

  • Barnhart MC (1986) Control of acid-base status in active and dormant land snails,Otala lactea (Pulmonata, Helicidae). J Comp Physiol B 156:347–354

    Article  Google Scholar 

  • Barnhart MC (1989) Respiratory acidosis and metabolic depression in dormant invertebrates. In: Malan A, Canguilhem B (eds) Living in the cold. John Libbey, pp 321–331

  • Barnhart MC, McMahon BR (1988) Depression of aerobic metabolism and intracellular pH by hypercapnia in land snails,Otalalactea. J Exp Biol 138:289–299

    Google Scholar 

  • Barnhart MC (1992) Acid-base regulation in pulmonate molluscs. J Exp Zool 263:120–126

    Article  CAS  Google Scholar 

  • Bergmeyer H (1985) Methods of enzymatic analysis, Vol VII. VCH Weinheim

    Google Scholar 

  • Brooks SPJ, Storey KB (1994) Metabolic depression in land snails: In vitro analysis of protein kinase involvement in pyruvate kinase control in isolatedOtala lactea tissues. J Exp Zool 269: 507–514

    Article  CAS  PubMed  Google Scholar 

  • Carpenter JF, Hand SC (1986) Arrestment of carbohydrate metabolism during anaerobic dormancy and aerobic acidosis inArtemia embryos: determination of pH-sensitive control points. J Comp Physiol B 156:451–459

    Article  CAS  Google Scholar 

  • Coulon-Bublex M, Dorel C (1991) The arrest of embryogenesis at gastrula state in the diapausing silkwormBombyx mori is related to the synthesis of protein P61. Roux's Arch Dev Biol 199: 469–475

    Article  CAS  Google Scholar 

  • Depocas F, Hart JS (1957) Use of the Pauling oxygen analyser for measurement of oxygen consumption of animals in open-circuit systems and in short-lag, closed circuit apparatus. J Appl Physiol 10:388–392

    CAS  PubMed  Google Scholar 

  • Doll CJ, Hochachka PW, Reiner PB (1991) Channel arrest: implications from membrane resistance in turtle neurones. Am J Physiol 261:R1321-R1324

    CAS  PubMed  Google Scholar 

  • Flanigan JE, Withers PC, Fuery CJ, Guppy M (1993) Metabolic depression and Na+/K+ gradients in the aestivating Australian goldfields frog,Neobatrachus wilsmorei. J Comp Physiol B 163: 587–593

    Article  CAS  PubMed  Google Scholar 

  • Flanigan JE, Withers PC, Guppy M (1991) In vitro metabolic depression of tissues from the aestivating frogNeobatrachus pelobatoides. J Exp Biol 161:273–283

    Google Scholar 

  • Fuery CJ, Withers PC, Hobbs A (1992) The role of protein synthesis in metabolic depression. Abstract Proc Aust Soc Biochem Mol Biol POS-2-6

  • Glasheen JS, Hand SC (1988) Anhydrobiosis in embryos of the brine shrimpArtemia: characterization of metabolic arrest during reductions in cell-associated water. J Exp Biol 135:363–380

    CAS  Google Scholar 

  • Goldbeter A, Koshland DE Jr (1987) Energy expenditure in the control of biochemical systems by covalent modification. J Biol Chem 262:4460–4471

    CAS  PubMed  Google Scholar 

  • Guppy M, Fuery CJ, Flanigan JE (1994) Biochemical principles of metabolic depression. Comp Biochem Physiol 109B:175–189

    CAS  Google Scholar 

  • Hand SC, Gnaiger E (1988) Anaerobic dormancy quantified inArtemia embryos: a calorimetric test of the control mechanism. Science 239:1425–1427

    CAS  Google Scholar 

  • Herreid CF (1977) Metabolism of land snails (Otala lactea) during dormancy, arousal and activity. Comp Biochem Physiol 56A: 211–215

    Google Scholar 

  • Hershey JWB (1989) Protein phosphorylation controls translation rates. J Biol Chem 264:20823–20826

    CAS  PubMed  Google Scholar 

  • Hofmann GE, Hand SC (1994) Global arrest of translation during invertebrate quiescence. Proc Natl Acad Sci USA 91: 8492–8496

    CAS  PubMed  Google Scholar 

  • Horne FR (1973) The utilization of food stuffs and urea production by a land snail during estivation. Biol Bull 144:321–330

    CAS  Google Scholar 

  • Isfort RJ, Cody DB, Asquith TN, Ridder GM, Stuard GM, Leboeuf RA (1993) Induction of protein phosphorylation, protein synthesis, immediate-early-gene expression and cellular proliferation by intracellular pH modulation. Eur J Biochem 213:349–357

    Article  CAS  PubMed  Google Scholar 

  • Jackson DC et al. (1991)31P-NMR study of normoxic and anoxic perfused turtle heart during graded CO2 and lactic acidosis. Am J Physiol 260:R1130-R1136

    CAS  PubMed  Google Scholar 

  • Joplin KH, Denlinger DL (1989) Cycles of protein synthesis during pupal diapause in the flesh flySarcophaga crassipalpis. Arch Insect Biochem Physiol 12:111–122

    Article  CAS  Google Scholar 

  • Kondo N, Kondo J (1992) Identification of novel blood proteins specific for mammalian hibernation. J Biol Chem 267:473–478

    CAS  PubMed  Google Scholar 

  • Machin J (1975) Water relationships. In: Fretter V, Peake J (eds) The pulmonates. Academic Press, New York, pp 105–163

    Google Scholar 

  • Malan A, Rodeau JL, Daull F (1985) Intracellular pH in hibernation and respiratory acidosis in the European hamster. J Comp Physiol B 156:251–258

    Article  CAS  PubMed  Google Scholar 

  • Midsukami M (1979) Physiological salines. The formulae for animals from protozoa to vertebrata. Keigaku, Tokyo

    Google Scholar 

  • Nestler JR (1990) Intracellular pH during daily torpor inPeromyscus maniculatus. J Comp Physiol 159:661–666

    CAS  Google Scholar 

  • Rees BB, Hand SC (1990) Heat dissipation, gas exchange and acidbase status in the land snailOreohelix during short-term estivation. J Exp Biol 152:77–92

    Google Scholar 

  • Rees BB, Hand SC (1991) Regulation of glycolysis in the land snailOreohelix during estivation and artificial hypercapnia. J Comp Physiol B 161:237–246

    Article  CAS  Google Scholar 

  • Rees BB, Malhotra D, Shapiro JI, Hand SC (1991) Intracellular pH decreases during entry into estivation in the land snailOreohelix strigosa. J Exp Biol 159:525–530

    Google Scholar 

  • Riddle WA (1977) Comparative respiratory physiology of a desert snail,Rabdotus schiedeanus, and a garden snail,Helix aspersa. Comp Biochem Physiol 56A:369–373

    Google Scholar 

  • Schmidt-Nielson K, Taylor CR, Sholnik A (1971) Desert snails: problems of heat, water and food. J Exp Biol 55:385–398

    Google Scholar 

  • Scholnick DA, Snyder GK, Spell AR (1994) Acid-Base status of a pulmonate land snail (Helix aspersa) and a prosobranch amphibious snail (Pomacea bridgesi) during dormancy. J Exp Zool 268:293–298

    Article  CAS  PubMed  Google Scholar 

  • Schulz JT, Cantley LC (1985) Characterization of an endogenous, membrane-bound kinase that phosphorylates the Na,K-ATPase in friend erythroleukemia cells. In: Glynn I, Ellory C (eds) The sodium pump. Charlesworth, Huddersfield, pp 689–694

    Google Scholar 

  • Storey KB (1993) Molecular mechanisms of metabolic arrest in molluscs. In: Hochachka PW, Lutz PL, Sick TJ, Rosenthal M, Thillart B v d. (eds) Surviving hypoxia: mechanism of control and adaptation. CRC Press, Boca Raton, pp 253–269

    Google Scholar 

  • Thomas MA, Agard JBR (1992) Metabolic rate depression in the ampullariid snailPomacea urceus (Müller) during aestivation and anaerobiosis. Comp Biochem Physiol 102A:675–678

    Google Scholar 

  • Vorhaben JE, Klotz AV, Campbell JW (1984) Activity and oxidative metabolism of the land snailHelix aspersal. Physiol Zool 57: 357–365

    CAS  Google Scholar 

  • Withers PC (1992) Comparative animal physiology. Saunders College Publishing, Fort Worth

    Google Scholar 

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Communicated by H. Huddart

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Pedler, S., Fuery, C.J., Withers, P.C. et al. Effectors of metabolic depression in an estivating pulmonate snail (Helix aspersa): whole animal and in vitro tissue studies. J Comp Physiol B 166, 375–381 (1996). https://doi.org/10.1007/BF02336920

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