Low-temperature protein metabolism: seasonal changes in protein synthesis and RNA dynamics in the Antarctic limpet Nacella concinna Strebel 1908
Tóm tắt
Protein synthesis is a fundamental and energetically expensive physiological process in all living organisms. Very few studies have examined the specific challenges of manufacturing proteins at low ambient temperatures. At high southern latitudes, water temperatures are continually below or near freezing and are highly stable, while food availability is very seasonal. To examine the effects of low temperature and a highly seasonal food supply on protein metabolism, we have measured wholebody protein synthesis, RNA concentrations, RNA:protein ratios and RNA translational efficiencies in the Antarctic limpet Nacella concinna at four times of the year. From summer to winter, protein synthesis rates decreased by 52%, RNA concentrations decreased by 55% and RNA:protein ratios decreased by 68%, while RNA translational efficiencies were low and very variable. Protein synthesis rates in N. concinna approached those measured in temperate mussels, while RNA:protein ratios were considerably higher than in temperate species. Interspecific comparisons show that species living at low temperatures have elevated RNA:protein ratios, which are probably needed to counteract a thermally induced reduction in RNA translational efficiency. Calculations using theoretical energetic costs of protein synthesis suggest that Antarctic species may allocate a larger proportion of their metabolic budget to protein synthesis than do temperate or tropical species.
Từ khóa
Tài liệu tham khảo
Arndt, S. K. A., Benfey, T. J. and Cunjak, R. A.(1996). Effect of temporary reductions in feeding on protein synthesis and energy storage of juvenile Atlantic salmon. J. Fish Biol.49,257-276.
Barnes, D. K. A. (1995). Seasonal and annual growth in erect species of Antarctic bryozoans. J. Exp. Mar. Biol. Ecol.188,181-198.
Barnes, D. K. A. and Clarke, A. (1994). Seasonal variation in the feeding activity of four species of Antarctic bryozoan in relation to environmental factors. J. Exp. Mar. Biol. Ecol.181,117-133.
Brêthes, J.-C., Ferreyra, G. and de la Vega, S.(1994). Distribution, growth and reproduction of the limpet Nacella (Patinigera) concinna (Strebel 1908) in relation to potential food availability, in Esperanza Bay (Antarctic Peninsula). Polar Biol.14,161-170.
Brockington, S. and Clarke, A. (2001). The relative influence of temperature and food on the metabolism of a marine invertebrate. J. Exp. Mar. Biol. Ecol.258, 87-99.
Brockington, S. and Peck, L. S. (2001). Seasonality of respiration and ammonium excretion in the Antarctic echinoid Sterechinus neumayeri.Mar. Ecol. Prog. Ser.219,159-168.
Bulow, F. J., Zeaman, M. E., Winningham, J. R. and Hudson, W. F. (1981). Seasonal variations in RNA—DNA ratios and in indicators of feeding, reproduction, energy storage, and condition in a population of bluegill, Lepomis macrochirus Rafinesque. J. Fish Biol.18,237-244.
Buttgereit, F. and Brand, M. D. (1995). A hierarchy of ATP-consuming processes in mammalian cells. Biochem. J.312,163-167.
Carter, C. G., Houlihan, D. F., Brechin, J. and McCarthy, I. D. (1993). The relationships between protein intake and protein accretion, synthesis, and retention efficiency for individual grass carp, Ctenopharyngodon idella (Valenciennes). Can. J. Zool.71,392-400.
Carter, C. G. and Houlihan, D. F. (2001). Protein synthesis. In Fish Physiology: Nitrogen Excretion, vol. 20 (ed. P. Wright and P. Anderson), pp. 31-75. London: Academic Press.
Clarke, A. (1983). Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr. Mar. Biol. Ann. Rev.21,341-453.
Clarke, A. and Johnston, N. M. (1999). Scaling of metabolic rate with body mass and temperature in teleost fish. J. Anim. Ecol.68,893-905.
Clarke, A., Rodhouse, P. G., Holmes, L. J. and Pascoe, P. L.(1989). Growth rate and nucleic acid ratio in cultured cuttlefish Sepia officinalis (Mollusca: Cephalopoda). J. Exp. Mar. Biol. Ecol.133,229-240.
Dayton, P. K. (1989) Interdecadal variation in an Antarctic sponge and its predators from oceanographic climate shifts. Science245,1484-1486.
Dayton, P. K., Robilliard, J. S., Paine, R. T. and Dayton, L. B. (1974). Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol. Monogr.44,105-128.
Detrich, H. W., III, Johnson, K. A. and Marchese-Ragona, S. P. (1989). Polymerization of Antarctic fish tubulins at low temperature: energetic aspects. Biochemistry28,10085-10093.
Fauconneau, B. and 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.
Foster, A. R., Houlihan, D. F. and Hall, S. J.(1993). Effects of nutritional regime on correlates of growth rate in juvenile Atlantic cod (Gadus morhua): comparison of morphological and biochemical measurements. Can. J. Fish Aquat. Sci.50,502-512.
Foster, A. R., Houlihan, D. F., Hall, S. J. and Burren, L. J. (1992). The effects of temperature acclimation on protein synthesis rates and nucleic acid content of juvenile cod (Gadus morhua L.). Can. J. Zool.70,2095-2102.
Fraser, K. P. P., Clarke, A. and Peck, L. S.(2002). Feast and famine in Antarctica: seasonal physiology in the limpet, Nacella concinna (Strebel 1908). Mar. Ecol. Prog. Ser., in press.
Fuery, C. J., Withers, P. C. and Guppy, M.(1998). Protein synthesis in the liver of Bufo marinus:cost and contribution to oxygen consumption. Comp. Biochem. Physiol.119A,459-467.
Garlick, P. J., McNurlan, M. A. and Preedy, V. R.(1980). A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H] phenylalanine. Biochem. J.192,719-723.
Goldspink, D. F. and Kelly, F. J. (1984). Protein turnover and growth in the whole body, liver and kidney of the rat from the foetus to senility. Biochem. J.217,507-516.
Haschemeyer, A. E. V. (1983). A comparative study of protein synthesis in nototheniids and icefish at Palmer station,Antarctica. Comp. Biochem. Physiol.76B,541-543.
Hawkins, A. J. S. (1985). Relationships between the synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel, Mytilus edulis L. Oecologia66,42-49.
Hawkins, A. J. S., Bayne, B. L. and Clarke, K. R.(1983). Co-ordinated rhythms of digestion, absorption and excretion in Mytilus edulis (Bivalvia: Mollusca). Mar. Biol.74,41-48.
Hewitt, D. R. (1992). Response of protein turnover in the brown tiger prawn Penaeus esculentus to variation in dietary protein content. Comp. Biochem. Physiol.103A,183-187.
Houlihan, D. F., Carter, C. G. and McCarthy, I. D.(1995a). Protein turnover in animals. In Nitrogen Metabolism and Excretion (ed. P. J. Walsh and P. Wright), pp.1-32. Boca Raton: CRC Press.
Houlihan, D. F., Carter, C. G. and McCarthy, I. D.(1995b). Protein synthesis in fish. In Biochemistry and Molecular Biology of Fishes, vol. 4(ed. P. Hochachka and T. Mommsen), pp. 191-220. Amsterdam: Elsevier Science.
Houlihan, D. F., Costello, M. J., Secombes, C. J., Stagg, R. and Brechin, J. (1994). Effects of sewage sludge exposure on growth, feeding and protein synthesis of Dab (Limanda limanda (L.)). Mar. Environ. Res.37,331-353.
Houlihan, D. F., McCarthy, I. D., Carter, C. G. and Marttin,F. (1995c). Protein turnover and amino acid flux in fish larvae. ICES Mar. Sci. Symp.201, 87-99.
Houlihan, D. F., McMillan, D. N., Agnisola, C., Genoino, I. T. and Foti, L. (1990). Protein synthesis and growth in Octopus vulgaris.Mar. Biol.106,251-259.
Houlihan, D. F., McMillan, D. N. and Laurent, P.(1986). Growth rates, protein synthesis, and protein degradation rates in rainbow trout: effects of body size. Physiol. Zool.59,482-493.
Johnston, I. A., Guderley, H. E., Franklin, C. E., Crockford, T. and Kamunde, C. (1994). Are mitochondria subject to evolutionary temperature adaptation? J. Exp. Biol.195,293-306.
Kent, J., Prosser, C. L. and Graham, G. (1992). Alterations in liver composition of channel catfish (Ictalurus punctatus) during seasonal acclimatization. Phy. Zool.65,867-884.
Kim, D. (2001). Seasonality of marine algae and grazers of an Antarctic rocky intertidal, with emphasis on the role of the limpet Nacella concinna Strebel (Gastropoda: Patellidae). Berichte Polar Meeresforschung. 397, 1-120.
Langar, H. and Guillaume, J. (1994). Effect of feeding pattern and dietary protein source on protein synthesis in European sea bass (Dicentrarchus labrax). Comp. Biochem. Physiol.108A,461-466.
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951). Protein measurement with the folin-phenol reagent. J. Biol. Chem.193,265-275.
Lyndon, A. R., Houlihan, D. F. and Hall, S. J.(1992). The effect of short-term fasting and a single meal on protein synthesis and oxygen consumption in cod, Gadus morhua.J. Comp. Physiol.B162,209-215.
Marsh, A. G., Maxson, R. E., Jr and Manahan, D. T.(2001). High macromolecular synthesis with low metabolic cost in Antarctic sea urchin embryos. Science291,1950-1952.
Mathers, E. M., Houlihan, D. F., McCarthy, I. D. and Burren, L. J. (1993). Rates of growth and protein synthesis correlated with nucleic acid content in fry of rainbow trout, Oncorhynchus mykiss: effects of age and temperature. J. Fish Biol.43,245-263.
McCarthy, I. D., Houlihan, D. F. and Carter, C. G.(1994). Individual variation in protein turnover and growth efficiency in rainbow trout, Oncorhynchus mykiss (Walbaum). Proc. R. Soc. Lond.B257,141-147.
Mejbaum, W. (1939). Über die bestimmung kleiner pentosemengen, insbesondere in derivaten der adenylsäure. Hoppe-Seyler's Z. Physiol. Chem.258,117-120.
Mente, E., Houlihan, D. F. and Smith, K.(2001). Growth, feeding frequency, protein turnover, and amino acid metabolism in European lobster Homarus gammarus L. J. Exp. Zool.289,419-432.
Millward, D. J., Garlick, P. J., James, W. P. T., Nnanyelugo, D. O. and Ryatt, J. S. (1973). Relationship between protein synthesis and RNA content in skeletal muscle. Nature241,204-205.
McNurlan, M. A., Tomkins, A. M. and Garlick, P. J.(1979). The effect of starvation on the rate of protein synthesis in rat liver and small intestine. Biochem. J.178,373-379.
O'Dor, R. K. and Wells, M. J. (1987). Energy and nutrient flow. In Cephalopod Life Cycles, vol.2 (ed. P. Boyle), pp. 109-134. London: Academic Press.
Peck, L. S., Brockington, S. and Brey, T.(1997). Growth and metabolism in the Antarctic brachiopod Liothyrella uva.Phil. Trans. R. Soc. Lond.B352,851-858.
Peck, L. S. and Conway, L. Z. (2000). The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. In The Evolutionary Biology of the Bivalvia(ed. E. M. Harper, J. D. Taylor and J. A. Crame), 177, pp. 441-450. London: Geological Society, Special Publications.
Picken, G. B. (1980). The distribution, growth,and reproduction of the Antarctic limpet Nacella (Patinigera)concinna (Strebel, 1908). J. Exp. Mar. Biol. Ecol.42,71-85.
Preedy, V. R., Paska, L., Sugden, P. H., Schofield, P. S. and Sugden, M. C. (1988). The effects of surgical stress and short-term fasting on protein synthesis in vivo in diverse tissues of the mature rat. Biochem. J.250,179-188.
Raae, A. J., Opstad, I., Kvenseth, P. and Walther, B. T.(1988). RNA, DNA and protein during early development of feeding and starved cod (Gadhus morhua L.) larvae. Aquaculture73,247-259.
Rauschert, M. (1991). Ergebnisse der faunistischen arbeiten im benthal von King George Island(Südshetlandinseln, Antarctis). Ber. Polarforsch.76, 1-75.
Ricker, W. E. (1979). Growth rates and models. In Fish Physiology, vol. 8 (ed. W. S. Hoar, D. J. Randall and J. R. Brett), pp.677-741. New York: Academic Press.
Robbins, I., Lubet, P. and Besnard, J.-Y.(1990). Seasonal variations in the nucleic acid content and RNA:DNA ratio of the gonad of the scallop Pecten maximus.Mar. Biol.105,191-195.
Robertson, R. F., El-Haj, A. J., Clarke, A. and Taylor, E. W. (2001a). Effects of temperature on specific dynamic action and protein synthesis rates in the Baltic isopod crustacean, Saduria entomon.J. Exp. Mar. Biol. Ecol.262,113-129.
Robertson, R. F., El-Haj, A. J., Clarke, A., Peck, L. S. and Taylor, E. W. (2001b). The effects of temperature on metabolic rate and protein synthesis following a meal in the isopod Glyptonotus antarcticus Eights (1852). Polar Biol.24,677-686.
Shabica, S. V. (1976). The natural history of the Antarctic limpet Patinigera polaris (Hombron and Jacquinot). PhD thesis, Oregon State University, USA.
Smith, M. A. K. and Haschemeyer, A. E. V.(1980). Protein metabolism and cold adaptation in Antarctic fishes. Physiol. Zool.53,373-382.
Sokal, R. R. and Rohlf, F. J. (1995). Biometry. Third edition. New York: W. H. Freeman and Co.
Tesseraud, S., Peresson, R. and Chagneau, A. M.(1996). Age-related changes of protein turnover in specific tissues of the chick. Poultry Sci.75,627-631.
Whiteley, N. M., Taylor, E. W. and El Haj, A. J.(1996). A comparison of the metabolic cost of protein synthesis in stenothermal and eurythermal isopod crustaceans. Am. J. Physiol.271,R1295-R1303.