Thermal plasticity of mitochondria: A latitudinal comparison between Southern Ocean molluscs

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 152, Issue 3, 2009, Pages 423-430

  Morley, Simon A ^a   Lurman, Glenn J ^a,b   Skepper, Jeremy N ^c   Pörtner, Hans Otto ^b   Peck, Lloyd S ^a  

^a BRITISH ANTARCTIC SURVEY   (United Kingdom)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Antarctica; Congeners; Cristae; Geographic comparisons; Laternula elliptica; Marine ectotherms; Mitochondrial density; Nacella concinna

Indexed keywords

CITRATE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTARCTICA; ARTICLE; CLAM; CONTROLLED STUDY; DENSITY; ENZYME ACTIVITY; LATERNULA ELLIPTICA; LATITUDE; LIFESTYLE; MITOCHONDRION; MOLLUSC; MUSCLE CELL; NACELLA CONCINNA; NONHUMAN; PLASTICITY; SURFACE PROPERTY; TEMPERATURE ACCLIMATIZATION;

ANIMALIA; BIVALVIA; LATERNULA ELLIPTICA; MOLLUSCA; NACELLA CONCINNA;

EID: 61349194395     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2008.11.015     Document Type: Article

References (66)

1. Barnes D.K.A., Linse K., Waller C., Morley S., Enderlein P., Fraser K.P.P., and Brown M. Shallow benthic fauna communities of South Georgia Island. Polar Biol. 29 (2005) 223-228
2. Barnes D.K.A., Fuentes V., Clarke A., Schloss I.R., and Wallace M.I. Spatial and temporal variation in sweater temperatures around Antarctica. Deep-Sea Res. II 53 (2006) 853-865
3. Boyle K.L., Dillaman R.M., and Kinsey S.T. Mitochondrial distribution and glycogen dynamics suggest diffusion constraints in muscle fibers of the blue crab, Callinectes sapidus. J. Exp. Zool. A: Comparative Experimental Biology 297A (2003) 1-16
4. Branch G.M. The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanogr. Mar. Biol. Ann. Rev. 19 (1981) 235-380
5. Brokordt K.B., Himmelman J.H., and Guderley H.E. Effect of reproduction on escape responses and muscle metabolic capacities in the scallop Chlamys islandica Müller 1776. J. Exp. Mar. Biol. Ecol. 251 (2000) 205-225
6. Brown K.M., Fraser K.P.F., Barnes D.K.A., and Peck L.S. Links between the structure of an Antarctic shallow-water community and ice-scour frequency. Oecologia 141 (2004) 121-129
7. Clarke A. Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr. Mar. Biol. 21 (1983) 341-453
8. Clarke A. Temperature and energetics: an introduction to cold ocean physiology. In: Pörtner H.O., and Playle R.C. (Eds). Cold Ocean Physiology. SEB Seminar Series vol. 66 (1998), Cambridge University Press, Cambridge 3-32
9. Clarke A., and Leakey R.J.G. The seasonal cycle of phytoplankton, macronutrients, and the microbial community in a nearshore Antarctic marine ecosystem. Limnol. Oceanogr. 41 (1996) 1281-1294
10. Clarke A., Meredith M.P., Wallace M.I., Brandon M.A., and Thomas D.N. Seasonal and interannual variability in temperature, chlorophyll and macronutrients in northern Marguerite Bay, Antarctica. Deep-Sea Res. -II 55 (2008) 1988-2006
11. Crockett L., and Sidell B.D. Some pathways of energy metabolism are cold adapted in Antarctic fishes. Physiol. Zool. 63 (1990) 472-488
12. Da Silva F.M., and Hodgson A.N. Fine-structure of the pedal muscle of the whelk Bullia-rhodostoma Reeve-correlation with function. Comp. Biochem. Physiol. A 87 (1987) 143-149
13. Davenport J.D. Comparisons of the biology of the intertidal Subantarctic limpets Nacella concinna and Kerguelenella lateralis. J. Moll. Stud. 63 (1997) 39-48
14. Dykens J.A., and Mangum C.P. The design of cardiac muscle and the mode of metabolism in molluscs. Comp. Biochem. Physiol. A 62 (1979) 549-554
15. Egginton S., and Sidell B.D. Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 256 (1989) R1-R9
16. Egginton S., Cordiner S., and Skilbeck C. Thermal compensation of peripheral oxygen transport in skeletal muscle of seasonally acclimatised trout. Am. J. Physiol. 279 (2000) R375-R388
17. Ellis E.A. New embedding formulations using Quetol 651. Microsc. Microanal. 8 (2002) 884-885
18. Forster M.E., Franklin C.E., Taylor H.H., and Davison W. The aerobic scope of an Antarctic fish, Pagothenia borchgrevinki and its significance for metabolic cold adaptation. Polar Biol. 8 (1987) 155-159
19. Guderley H.E. Metabolic response to low temperature in fish muscle. Biol. Rev. 79 (2004) 409-427
20. Guderley H.E. Locomotor performance and muscle metabolic capacities: impact of temperature and energetic status. Comp. Biochem. Physiol. B 139 (2004) 371-382
21. Guderley H.E., and Blier P. Thermal acclimation in fish: conservative and labile properties of swimming muscle. Can. J. Zool. 66 (1988) 1105-1115
22. Guderley H.E., and St. Pierre J. Phenotypic plasticity and evolutionary adaptations of mitochondria to temperature. In: Johnston I.A., and Bennet A. (Eds). Animals and Temperature. Soc. Exp. Biol. Semin. Ser. vol. 59 (1996) 127-152
23. Guderley H.E., and St. Pierre J. Going with the flow of life in the fast lane: contrasting mitochondrial responses to thermal change. J. Exp. Biol. 205 (2002) 2237-2249
24. Harper E.S., and Peck L.S. Predatory behaviour and metabolic costs in the Antarctic muricid gastropod Trophon longstaffi. Polar Biol. 26 (2003) 208-217
25. Hochachka P.W., and Somero G.N. Strategies of Biochemical Adaptation (1973), W.B. Saunders, Philadelphia
26. Hoppeler H. The range of mitochondrial adaptations in muscle fibres. In: Pette D. (Ed). The Dynamic State of Muscle Fibers (1990), Walter de Gruyter & Co, Berlin 567-586
27. Johnson L.K., Dillaman R.M., Gay D.M., Blum J.E., and Kinsey S.T. Metabolic influences of fiber size in aerobic and anaerobic locomotor muscles of the blue crab, Callinectes sapidus. J. Exp. Biol. 207 (2004) 4045-4056
28. Johnston I.A. Respiratory characteristics of muscle fibres in a fish (Chaenocephalus aceratus) that lack heam pigments. J. Exp. Biol. 133 (1987) 415-428
29. Johnston I.A., and Maitland B. Temperature acclimation in crucian carp (Carassius carassius L): morphometric analysis of muscle fibre ultrastructure. J. Fish. Biol. 17 (1980) 113-125
30. Johnston I.A., Calvo J.C., Guderley H., Fernandez D., and Palmer L. Latitudinal variation in the abundance and oxdative capacities of muscle mitochondria in perciform fishes. J. Exp. Biol. 201 (1998) 1-12
31. Josephine R.K. Extensive and intensive factors determining the performance of striated muscle. J. Exp. Zool. 194 (1975) 135-154
32. Kinsey S.T., Hardy K.M., and Locke B.R. The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle. J. Exp. Biol. 210 (2007) 3505-3512
33. Magwere T., Goodall S., Skepper J., Mair W., Brand M.D., and Partridge L. The effect of dietary restriction on mitochondrial protein density and flight muscle mitochondrial morphology in Drosophila. J. Geront. 61A (2006) 36-47
34. Morley S.A., Peck L.S., Miller A.J., and Pörtner H.O. Hypoxia tolerance associated with activity reduction is a key adaptation for Laternula elliptica seasonal energetics. Oecologia 153 (2007) 29-36
35. Morley S.A., Peck L.S., Tan K.S., Martin S.M., and Pörtner H.O. Slowest of the slow: latitudinal insensitivity of burrowing capacity in the bivalve Laternula. Mar. Biol. 151 (2007) 1823-1830
36. O'Brien K.M., Skilback C., Sidell B.D., and Egginton S. Muscle fine structure may maintain the function of oxidative fibres in haemoglobinless Antarctic fishes. J. Exp. Biol. 206 (2003) 411-421
37. Peck L.S. Prospects for survival in the Southern Ocean: vulnerability of benthic species to temperature change. Ant. Sci. 4 (2005) 497-507
38. Peck L.S., and Conway L.Z. The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. In: Harper E.M., Taylor J.D., and Crame J.A. (Eds). The Evolutionary Biology of the Bivalvia. Special Publications vol. 177 (2000), The Geological Society of London, London 441-450
39. Peck L.S., Pörtner H.O., and Hardewig I. Metabolic demand, oxygen supply, and critical temperatures in the Antarctic bivalve Laternula elliptica. Physiol. Bioch. Zool. 75 (2002) 123-133
40. Peck L.S., Webb K.E., and Bailey D.M. Extreme sensitivity of biological function to temperature in Antarctic species. Func. Ecol. 18 (2004) 625-630
41. Peck L.S., Ansell A.D., Webb K.E., Hepburn L., and Burrows M.T. Movements and burrowing activity in the Antarctic bivalve molluscs Laternula elliptica and Yoldia eightsi. Polar Biol. 27 (2004) 357-367
42. Peck L.S., Convey P., and Barnes D.K.A. Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biol. Rev. 81 (2006) 75-109
43. Peck L.S., Webb K.E., Miller A., Clark M.S., and Hill T. Temperature limits to activity, feeding and metabolism in the Antarctic starfish Odontaster validus. Mar. Ecol. Prog. Ser. 358 (2008) 181-189
44. Peck, L.S., Clark, M.S., Morley, S.A., Massey, A., Rossetti, H., in press. Animal temperature limits and ecological relevance: effects of size, activity and rates of change. Func. Ecol.
45. Philipp E.E.R., Schmidt M., Gsottbauer C., Sänger A.M., and Abele D. Size- and age-dependent changes in adductor muscle swimming physiology of the scallop Aequipecten opercularis. J. Exp. Biol. 211 (2008) 2492-2501
46. Plesch B. An ultrastructural study of the musculature of the pond snail Lymnaea stagnalis L. Cell Tissue Res. 180 (1977) 317-340
47. Pörtner H.O. Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp. Biochem. Physiol. A 132 (2002) 739-761
48. Pörtner H.O. Physiological basis of temperature-dependant biogeography: trade-offs in muscle design and performance in polar ectotherms. J. Exp. Biol. 205 (2002) 2217-2230
49. Pörtner H.O. Climate dependent evolution of Antarctic ectotherms: an integrative analysis. Deep-Sea Res. II 53 (2006) 1071-1104
50. Pörtner H.O., van Dijk P.L.M., Hardewig I., and Sommer A. Levels of metabolic cold adaptation: tradeoffs in eurythermal and stenothermal ectotherms. In: Davison W., and Williams C.H. (Eds). Antarctic Ecosystems: Models for Wider Ecological Understanding (2000), Caxton Press, Christchurch 109-122
51. Rolfe D.F.S., Newman J.M.B., Buckingham J.A., Clark M.G., and Brand M.D. Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am. J. Physiol. 276 (1999) C692-C699
52. Santini G., and Chelazzi G. Glycogen content and rates of depletion in two limpets with different foraging regimes. Comp. Biochem. Physiol. 111A (1995) 271-277
53. Seebacher F., Davison W., Lowe C.J., and Franklin C.E. A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fish. Biol. Lett. 1 (2005) 151-154
54. Sidell B.D. Cellular acclimatisation to environmental change by quantitative alterations in enzymes and organelles. In: Cossins A.R., and Sheterline P. (Eds). Cellular Acclimatisation to Environmental Change (1983), Cambridge University Press, London 103-120
55. Sidell B.D., and Hazel J.R. Temperature affects the diffusion of small molecules through cytosol of fish muscle. J. Exp. Biol. 129 (1987) 191-203
56. Sidell B.D., Driedzic W.R., Stowe D.B., and Johnston I.A. Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol. Zool. 60 (1987) 221-232
57. Sommer A.M., and Pörtner H.O. Metabolic cold adaptation in the lugworm Arenicola marina: comparison of a North Sea and White Sea population. Mar. Ecol. Prog. Ser. 240 (2002) 171-182
58. Stillman J.H. Acclimation capacity underlies susceptibility to climate change. Science 301 (2003) 65
59. St-Pierre J., Charest P.M., and Guderley H.E. Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimation of rainbow trout, Oncorhynchus mykiss. J. Exp. Biol. 201 (1998) 2961-2970
60. Suarez R.K. Energy metabolism during insect flight: biochemical design and physiological performance. Physiol. Biochem. Zool. 73 (2000) 765-771
61. Van Dijk P.L.M., Hardewig I., and Pörtner H.O. Exercise in the cold: high energy turnover in Antarctic fish. In: di Prisco G., Pisano E., and Clarke A. (Eds). Fishes of Antarctica: A Biological Overview (1998), Springer, Berlin 225-236 Heidelberg, New York
62. Van den Thillart G., and Modderkolk J. Effect of acclimation temperature on activation-energies of state III respiration and on unsaturation of membrane lipids of goldfish mitochondria. Biochem. Biophys. Acta 510 (1978) 38-51
63. Waller C.L., Worland M.R., Convey P., and Barnes D.K.A. Ecophysiological strategies of Antarctic intertidal invertebrates faced with freezing stress. Polar Biol. 26 (2006) 1077-1083
64. Watson A.L., Skepper J.N., Jauniaux E., and Burton G.J. Susceptibility of human placental syncytiotrophoblastic mitochondria to oxygen-mediated damage in relation to gestational age. J. Clin. Endocrinol. and Metab. 83 (1998) 1697-1705
65. Weibel E.R. Stereological Methods (1979), Academic Press Inc, London
66. Williams M.A. Quantitative methods in biology. In: Glauert A.M. (Ed). Practical Methods in Electron Microscopy 6 (1977), New Holland Publishing Company