Skip to main content
SpringerLink
Log in

Protein synthesis and growth inOctopus vulgaris

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Rates of protein synthesis in the whole body and tissues ofOctopus vulgaris collected in September 1985 and 1986 from the Bay of Naples were measured following a flooding dose injection of3H phenylalanine. There were stable phenylalanine free pool-specific radioactivities and linear incorporation of radiolabel into arm-tip protein from 10 to 30 min after the injection. In starved individuals there were no significant differences between the fractional rates of protein synthesis of the following tissues: ventricle, brain, branchial heart, arm tip, gill, stomach, arm, renal appendage and mantle. The mean value (± SE) for all the tissues was 3.02 ± 0.17% d−1. In individuals fed varying amounts of crab, resulting in differing growth rates, there was a linear increase in fractional rates of whole-body protein synthesis with growth rate. A standard 148 g octopus growing at 3.0% d−1 synthesised 0.54 g of protein, with 0.43 g of this protein retained as growth. The proportion of the total protein synthesis which was retained as growth increased with increasing growth rate; at a maximum growth rate of 6% d−1, over 90% of the protein synthesised was retained as growth. The ventricle, arm tip, gill, arm and mantle also showed similar patterns of a linear increase in fractional rates of protein synthesis with increased growth rates. The RNA concentrations in the whole body and tissues increased with increasing growth rates, but the major change was an increase in the efficiency of translation. It is concluded that rapid growth rates inO. vulgaris are brought about by high rates of protein synthesis and high efficiencies of retention of synthesised protein and, therefore, little protein degradation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Aoyagi, Y., Tasaki, I., Okumura, J.-I., Muramatsu, T. (1988). Energy cost of whole-body protein synthesis measuredin vivo in chicks. Comp. Biochem. Physiol. 91A: 765–768

    Google Scholar 

  • Ashford, A. J., Pain, V. M. (1986). Effects of diabetes on the rates of synthesis and degradation of ribosomes in rat muscle and liverin vivo. J. biol. Chem. 261: 4059–4065

    Google Scholar 

  • Bates, P. C., Millward, D. J. (1981). Characteristics of skeletal muscle growth and protein turnover in a fast-growing rat strain. Br. J. Nutr. 46: 7–13

    Google Scholar 

  • Boucher-Rodoni, R., Boucaud-Camou, E., Mangold, K. (1987). Feeding and digestion. In: Boyle, P. R. (ed.) Cephalopod life cycles. Vol 2. Academic Press, London, p. 85–108

    Google Scholar 

  • Boyle, P. R., Knobloch, D. (1982). On growth of the octopusEledone cirrhosa. J. mar. biol. Ass. U.K. 62: 277–296

    Google Scholar 

  • Buckley, L. J. (1984). RNA-DNA ratio: an index of larval fish growth in the sea. Mar. Biol. 80: 291–298

    Google Scholar 

  • Calow, P. (1985). Adaptive aspects of energy allocation. In: Tytler, P., Calow, P. (eds.) Fish energetics: new perspectives. Croom Helm, London, p. 13–32

    Google Scholar 

  • Calow, P. (1987). Fact and theory — an overview. In: Boyle, P. R. (ed.) Cephalopod life cycles. Vol. 2. Academic Press, London, p. 351–366

    Google Scholar 

  • Calow, P., Townsend, C. R. (1981). Resource utilisation in growth. In: Townsend, C. R., Calow, P. (eds.). Physiological ecology. Oxford, Blackwell Scientific, p. 220–244

    Google Scholar 

  • Fauconneau, B. (1985). Protein synthesis and protein deposition in fish. In: Cowey, C. B., Mackie, A. E., Bell, J. G. (eds.). Nutrition and feeding in fish. Academic Press, London, p. 17–45

    Google Scholar 

  • Fauconneau, B., Arnal, M. (1985).In vivo protein synthesis in different tissues and the whole body of rainbow trout (Salmo gairdnerii R). Influence of environmental temperature. Comp. Biochem. Physiol. 82A: 179–187

    Google Scholar 

  • Florkin, M., Bricteux-Gregoire, S. (1972). Nitrogen metabolism in molluscs. In: Florkin, M., Scheer, B. T. (eds.). Chemical zoology. Vol. 7. Academic Press, New York, p. 301–348

    Google Scholar 

  • Forsythe, J. W., van Heukelem, W. F. (1987). Growth. In: Boyle, P. R. (ed.). Cephalopod life cycles. Vol. 2. Academic Press, London, p. 135–156

    Google Scholar 

  • Garlick, P. J. (1980). Assessment of protein metabolism in the intact animal. In: Buttery, P. J., Lindsay, D. B. (eds). Protein deposition in animals. Butterworths, London, p. 77–152

    Google Scholar 

  • Garlick, P. J., Burk, T. L., Swick, R. W. (1976). Protein synthesis and RNA in tissues of the pig. Am. J. Physiol. 230: 1108–1112

    Google Scholar 

  • Garlick, P. J., Fern, M., Preedy, V. R. (1983). The effect of insulin infusion and food intake on muscle protein synthesis in post-absorptive rats. Biochem. J. 210: 669–676

    Google Scholar 

  • Garlick, P. J., McNurlan, M. A., Preedy, V. R. (1980). A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of3H phenylalanine. Biochem. J. 192: 719–723

    Google Scholar 

  • Goldspink, D. F., Kelly, F. J. (1984). Protein turnover and growth in the whole body, liver and kidney of the rat from foetus to senility. Biochem. J. 217: 507–516

    Google Scholar 

  • Harmon, C. S., Park, J. H. (1987). Stimulation of epidermal protein synthesisin vivo by topical triamcinolone acetonide. Biochem. J. 247: 525–530

    Google Scholar 

  • Haschemeyer, A. E. V., Persell, R., Smith, M. A. K. (1979). Effect of temperature on protein synthesis in fish of the Galapagos and Perlas Islands. Comp. Biochem. Physiol. 64B: 91–95

    Google Scholar 

  • Haschemeyer, A. E. V., Smith, M. A. K. (1979). Protein synthesis in liver, muscle and gill of mullet (Mugil cephalus L.)in vivo. Biol. Bull. mar. biol. Lab., Woods Hole 156: 93–102

    Google Scholar 

  • Hawkins, A. J. S. (1985). Relationships between synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel,Mytilus edulis L. Oecologia 66: 42–49

    Google Scholar 

  • Hershko, A., Ciechanover, A. (1982). Mechanisms of intracellular protein breakdown. A. Rev. Biochem. 51: 335–364

    Google Scholar 

  • Houlihan, D. F., Hall, S. J., Gray, C. (1989). Effects of ration on protein turnover in cod. Aquaculture, Amsterdam 79: 103–110

    Google Scholar 

  • Houlihan, D. F., Hall, S. J., Gray, C., Noble, B. S. (1988). Growth rates and protein turnover in Atlantic cod,Gadus morhua. Can. J. Fish. aquat. Sciences 43: 951–964

    Google Scholar 

  • Houlihan, D. F., Laurent, P. (1987). Effect of exercise training on the performance, growth and protein turnover of rainbow trout (Salmo gairdneri). Can. J. Fish. aquat. Sciences 44: 1614–1621

    Google Scholar 

  • Houlihan, D. F., McMillan, D. N., Laurent, P. (1986). Growth rates, protein synthesis and protein degradation rates in rainbow trout: effects of body size. Physiol. Zoöl. 59: 482–493

    Google Scholar 

  • Kariya, Y., Ochiai, Y., Hashimoto, K. (1986). Protein components and ultrastructure of the arm and mantle ofOctopus vulgaris. Bull. Jap. Soc. scient. Fish. 52: 131–138

    Google Scholar 

  • Loughna, P. T., Goldspink, G. (1984). The effects of starvation upon protein turnover in red and white myotomal muscle of rainbow trout,Salmo gairdneri Richardson. J. Fish Biol. 25: 223–230

    Google Scholar 

  • Love, R. M. (1980). The chemical biology of fishes. Vol II. Academic Press, New York

    Google Scholar 

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. biol. Chem. 193: 265–275

    Google Scholar 

  • Mangold, K. (1983).Octopus vulgaris. In: Boyle, P. R. (ed.). Cephalopod life cycles. Vol. 1. Academic Press, London, p. 335–364

    Google Scholar 

  • Mangold, K., Boletzky, S. von (1973). New data on reproductive biology and growth ofOctopus vulgaris. Mar. Biol. 19: 7–12

    Google Scholar 

  • McMillan, D. N., Houlihan, D. F. (1988). The effect of re-feeding on tissue protein synthesis in rainbow trout. Physiol. Zöol. 61: 429–441

    Google Scholar 

  • Millward, D. J., Brown, J. G., Odedra, G. (1981). Protein turnover in individual tissues with special emphasis on muscle. In: Waterlow, J. C., Stephen, J. M. L. (eds.) Nitrogen metabolism in man, Applied Science Publishers, London, p. 475–496

    Google Scholar 

  • Millward, D. J., Garlick, P. J., James, W. P. T., Nnantelugo, D. O., Ryatt, J. S. (1973). Relationship between protein synthesis and RNA content in skeletal muscle. Nature, Lond. 241: 204–205

    Google Scholar 

  • Mommsen, T. P., Ballantyne, J., MacDonald, D., Gosline, J., Hochachka, P. W. (1981). Analogues of red and white muscle in squid muscle. Proc. natn. Acad. Sci. U.S.A. 78: 3274–3278

    Google Scholar 

  • Munro, H. N. (1969). Evolution of protein metabolism in mammals. In: Munro, H. N. (ed.) Mammalian protein metabolism. Vol. 111. Academic Press, New York, p. 133–182

    Google Scholar 

  • Munro, H. N., Fleck, A. (1966). The determination of nucleic acids. In: Glick, D. (ed.) Methods of biochemical analysis. Vol. 14. Wiley, New York, p. 113–176

    Google Scholar 

  • Munro, H. N., Gray, J. A. M. (1969). The nucleic acid content of skeletal muscle and liver in mammals of different body size. Comp. Biochem. Physiol. 28: 897–905

    Google Scholar 

  • O'Dor, R. K., Wells, M. J. (1973). Yolk protein synthesis in the ovary ofOctopus vulgaris and its control by the optic gland gonadotropins. J. exp. Biol. 59: 665–674

    Google Scholar 

  • O'Dor, R. K., Wells, M. J. (1978). Reproduction versus somatic growth: hormonal control inOctopus vulgaris. J. exp. Biol. 77: 15–31

    Google Scholar 

  • O'Dor, R. K., Wells, M. J. (1987). Energy and nutrient flow. In: Boyle, P. R. (ed.). Cephalopod life cycles. Vol. 2. Academic Press, London, p. 109–134

    Google Scholar 

  • Pocrnjic, Z., Mathews, R. W., Rappaport, S., Haschemeyer, A. E. V. (1983). Quantitative protein synthetic rates in various tissues of a temperate fishin vivo by the method of phenylalanine swamping. Comp. Biochem. Physiol. 74B: 735–738

    Google Scholar 

  • Preedy, V. R., Paska, L., Sugden, P. H., Schofield, P. S., Sugden, M. C. (1988). The effects of surgical stress and short-term fasting on protein synthesisin vivo in diverse tissues of the mature rat. Biochem. J. 250: 179–188

    Google Scholar 

  • Reeds, P. J., Fuller, M. F., Nicholson, B. A. (1985). Metabolic basis of energy expenditure with particular reference to protein. In: Garrow, J. S., Halliday, D. (eds.). Substrate and energy metabolism in man. John Libbey, London, p. 46–57

    Google Scholar 

  • Ricker, W. E. (1979). Growth rates and models. In: Hoar, W. S., Randall, D. J., Brett, J. R. (eds.). Fish physiology. Vol. 8. Academic Press, New York, p. 677–743

    Google Scholar 

  • Smith, M. A. K. (1981). Estimation of growth potential by measurement of tissue protein synthesis rates in feeding and fasting rainbow trout,Salmo gairdneri. J. Fish Biol. 19: 213–220

    Google Scholar 

  • Smith, M. A. K., Mathews, R. W., Hudson, A. P., Haschemeyer, A. E. V. (1980). Protein metabolism of tropical reef and pelagic fish. Comp. Biochem. Physiol. 65B: 415–418

    Google Scholar 

  • Snedecor, G. W., Cochran, W. G. (1976). Statistical methods. 6th ed. Iowa State University Press, Ames, Iowa

    Google Scholar 

  • Storey, K. B., Storey, J. M. (1983). Carbohydrate metabolism in cephalopod molluscs. In: Hochachka, P. W. (ed.) The molluscs. Vol. 1. Academic Press, New York, p. 92–137

    Google Scholar 

  • Waterlow, J. C. (1984). Protein turnover with special reference to man. Q. Jl exp. Physiol. 69: 409–438

    Google Scholar 

  • Wells, M. J., O'Dor, R. K., Mangold, K., Wells, J. (1983). Feeding and metabolic rate inOctopus vulgaris. Mar. behav. Physiol. 9: 305–317

    Google Scholar 

  • Yacoe, M. E. (1982). Protein metabolism in the pectoralis muscle and liver of hibernating bats,Eptesicus fuscus. J. comp. Physiol. (Sect. B) 152: 137–144

    Google Scholar 

  • Young, V. R. (1970). The role of skeletal and cardiac muscle in the regulation of protein metabolism. In: Munro, H. N. (ed.) Mammalian protein metabolism. Vol. 4. Academic Press, London, p. 585–674

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Aberdeen, AB9 2TN, Aberdeen, Scotland

    D. F. Houlihan & D. N. McMillan

  2. Stazione Zoologica “Anton Dohrn”, I-80121, Napoli, Italy

    C. Agnisola

  3. Department of General and Environmental Physiology, University of Naples, I-80134, Napoli, Italy

    C. Agnisola, I. Trara Genoino & L. Foti

Authors
  1. D. F. Houlihan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. N. McMillan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Agnisola
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. Trara Genoino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Foti
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. Mauchline, Oban

Rights and permissions

Reprints and permissions

About this article

Cite this article

Houlihan, D.F., McMillan, D.N., Agnisola, C. et al. Protein synthesis and growth inOctopus vulgaris . Mar. Biol. 106, 251–259 (1990). https://doi.org/10.1007/BF01314808

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01314808

Keywords

Search

Navigation