Rapid Mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oyster, Crassostrea gigas

Journal of Experimental Biology

Volumn 216, Issue 9, 2013, Pages 1561-1569

  Sussarellu, Rossana ^a   Dudognon, Tony ^a   Fabioux, Caroline ^a   Soudant, Philippe ^a   Moraga, Dario ^a   Kraffe, Edouard ^a  

^a INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

Author keywords

Alternative oxidase; Hypoxia; Mitochondria; Oyster; Re oxygenation; Respiration

Indexed keywords

ALTERNATIVE OXIDASE; CYTOCHROME; CYTOCHROME C OXIDASE; MESSENGER RNA; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; OXYGEN; VEGETABLE PROTEIN;

ANAEROBIC GROWTH; ANIMAL; ARTICLE; CELL RESPIRATION; CRASSOSTREA; DIGESTIVE SYSTEM; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GILL; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; PACIFIC OCEAN; PHOSPHORYLATION; TIME;

ANAEROBIOSIS; ANIMALS; CELL RESPIRATION; CRASSOSTREA; CYTOCHROMES; DIGESTIVE SYSTEM; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GILLS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDOREDUCTASES; OXYGEN; OXYGEN CONSUMPTION; PACIFIC OCEAN; PHOSPHORYLATION; PLANT PROTEINS; RNA, MESSENGER; TIME FACTORS;

CRASSOSTREA GIGAS; OSTREIDAE;

EID: 84876859968     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.075879     Document Type: Article

References (64)

1. Abele, E., Philip, E., Gonzalez, P. M. and Puntarulo, S. (2007). Marine invertebrate mitochondria and oxidative stress. Front. Biosci. 12, 933-946.
2. Albury, M. S., Elliott, C. and Moore, A. L. (2010). Ubiquinol-binding site in the alternative oxidase: mutagenesis reveals features important for substrate binding and inhibition. Biochim. Biophys. Acta 1797, 1933-1939.
3. 2 uptake by wheat roots. Physiol. Plant. 93, 427-434.
4. Bishop, T., St-Pierre, J. and Brand, M. D. (2002). Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells. Am. J. Physiol. 282, R372-R382.
5. Blier, P. U. and Lemieux, H. (2001). The impact of the thermal sensitivity of cytochrome c oxidase on the respiration rate of Arctic charr red muscle mitochondria. J. Comp. Physiol. B 171, 247-253.
6. Bouchard, P. and Guderley, H. (2003). Time course of the response of mitochondria from oxidative muscle during thermal acclimation of rainbow trout, Oncorhynchus mykiss. J. Exp. Biol. 206, 3455-3465.
7. Brand, M. D. (2000). Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp. Gerontol. 35, 811-820.
8. Bremer, K. and Moyes, C. D. (2011). Origins of variation in muscle cytochrome c oxidase activity within and between fish species. J. Exp. Biol. 214, 1888-1895.
9. Bridges, C. R., Taylor, A. C., Morris, S. J. and Grieshaber, M. K. (1984). Ecophysiological adaptations in Blennius pholis (L.) blood to intertidal rockpool environments. J. Exp. Mar. Biol. Ecol. 77, 151-167.
10. Buchner, T., Abele, D. and Pörtner, H.-O. (2001). Oxyconformity in the intertidal worm Sipunculus nudus: the mitochondrial background and energetic consequences. Comp. Biochem. Physiol. 129B, 109-120.
11. Burcham, J., Paynter, K. and Bishop, S. (1983). Coupled mitochondria from oyster gill tissue. Mar. Biol. Lett. 4, 348-356.
12. Buttemer, W. A., Abele, D. and Costantini, D. (2010). From bivalves to birds: oxidative stress and longevity. Funct. Ecol. 24, 971-983.
13. Chance, B. and Williams, G. R. (1956). Respiratory chain and oxidative phosphorylation. In Advances in Enzymology and Related Areas of Molecular Biology (ed. F. F. Nord), pp. 65-130. Hoboken, NJ: John Wiley & Sons.
14. Chandel, N., Budinger, G. R., Kemp, R. A. and Schumacker, P. T. (1995). Inhibition of cytochrome-c oxidase activity during prolonged hypoxia. Am. J. Physiol. 268, L918-L925.
15. Chandel, N. S., Budinger, G. R. S. and Schumacker, P. T. (1996). Molecular oxygen modulates cytochrome c oxidase function. J. Biol. Chem. 271, 18672-18677.
16. Chandel, N. S., Budinger, G. R. S., Choe, S. H. and Schumacker, P. T. (1997). Cellular respiration during hypoxia. Role of cytochrome oxidase as the oxygen sensor in hepatocytes. J. Biol. Chem. 272, 18808-18816.
17. Cloern, J. E. (2001). Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser. 210, 223-253.
18. David, E., Tanguy, A., Pichavant, K. and Moraga, D. (2005). Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J. 272, 5635-5652.
19. Dheilly, N. M., Lelong, C., Huvet, A. and Favrel, P. (2011). Development of a Pacific oyster (Crassostrea gigas) 31, 918-feature microarray: identification of reference genes and tissue-enriched expression patterns. BMC Genomics 12, 468.
20. Donaghy, L., Kraffe, E., Le Goïc, N., Lambert, C., Volety, A. K. and Soudant, P. (2012). Reactive oxygen species in unstimulated hemocytes of the pacific oyster Crassostrea gigas: a mitochondrial involvement. PLoS ONE 7, e46594.
21. Duerr, J. M. and Podrabsky, J. E. (2010). Mitochondrial physiology of diapausing and developing embryos of the annual killifish Austrofundulus limnaeus: implications for extreme anoxia tolerance. J. Comp. Physiol. B 180, 991-1003.
22. Fabioux, C., Huvet, A., Lelong, C., Robert, R., Pouvreau, S., Daniel, J. Y., Minguant, C. and Le Pennec, M. (2004). Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem. Biophys. Res. Commun. 320, 592-598.
23. Frick, N. T., Bystriansky, J. S., Ip, Y. K., Chew, S. F. and Ballantyne, J. S. (2010). Cytochrome c oxidase is regulated by modulations in protein expression and mitochondrial membrane phospholipid composition in estivating African lungfish. Am. J. Physiol. 298, R608-R616.
24. Gerson, A. R., Brown, J. C. L., Thomas, R., Bernards, M. A. and Staples, J. F. (2008). Effects of dietary polyunsaturated fatty acids on mitochondrial metabolism in mammalian hibernation. J. Exp. Biol. 211, 2689-2699.
25. Gnaiger, E., Lassnig, B., Kuznetsov, A., Rieger, G. and Margreiter, R. (1998). Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J. Exp. Biol. 201, 1129-1139.
26. Gray, J. S., Wu, R. S. and Or, Y. Y. (2002). Effects of hypoxia and organic enrichment on the coastal marine environment. Mar. Ecol. Prog. Ser. 238, 249-279.
27. Grieshaber, M. K., Hardewig, I., Kreutzer, U. and Pörtner, H. O. (1994). Physiological and metabolic responses to hypoxia in invertebrates. Rev. Physiol. Biochem. Pharmacol. 125, 43-147.
28. Groen, A. K., Wanders, R. J., Westerhoff, H. V., van der Meer, R. and Tager, J. M. (1982). Quantification of the contribution of various steps to the control of mitochondrial respiration. J. Biol. Chem. 257, 2754-2757.
29. Guderley, H. (2004). Locomotor performance and muscle metabolic capacities: impact of temperature and energetic status. Comp. Biochem. Physiol. 139B, 371-382.
30. Guderley, H., Turner, N., Else, P. L. and Hulbert, A. J. (2005). Why are some mitochondria more powerful than others: insights from comparisons of muscle mitochondria from three terrestrial vertebrates. Comp. Biochem. Physiol. 142B, 172-180.
31. Gueguen, Y., Cadoret, J.-P., Flament, D., Barreau-Roumiguière, C., Girardot, A.-L., Garnier, J., Hoareau, A., Bachère, E. and Escoubas, J.-M. (2003). Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteriachallenged oyster, Crassostrea gigas. Gene 303, 139-145.
32. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. and Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
33. Hochachka, P. W. and Lutz, P. L. (2001). Mechanism, origin, and evolution of anoxia tolerance in animals. Comp. Biochem. Physiol. 130B, 435-459.
34. Hochachka, P. W., Buck, L. T., Doll, C. J. and Land, S. C. (1996). Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc. Natl. Acad. Sci. USA 93, 9493-9498.
35. Kern, B., Ivanina, A. V., Piontkivska, H., Sokolov, E. P. and Sokolova, I. M. (2009). Molecular characterization and expression of a novel homolog of uncoupling protein 5 (UCP5) from the eastern oyster Crassostrea virginica (Bivalvia: Ostreidae). Comp. Biochem. Physiol. 4D, 121-127.
36. Kraffe, E., Marty, Y. and Guderley, H. (2007). Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J. Exp. Biol. 210, 149-165.
37. Kraffe, E., Tremblay, R., Belvin, S., Le Coz, J.-R., Marty, Y. and Guderley, H. (2008). Effect of reproduction on escape responses, metabolic rates and muscle mitochondrial properties in the scallop Placopecten magellanicus. Mar. Biol. 156, 25-38.
38. Kurochkin, I. O., Ivanina, A. V., Eilers, S., Downs, C. A., May, L. A. and Sokolova, I. M. (2009). Cadmium affects metabolic responses to prolonged anoxia and reoxygenation in eastern oysters (Crassostrea virginica). Am. J. Physiol. 297, R1262-R1272.
39. Larade, K. and Storey, K. B. (2002). A profile of the metabolic responses to anoxia in marine invertebrates. In Sensing, Signaling and Cell Adaptation (ed. K. B. Storey and J. M. Storey), pp. 27-46. Amsterdam: Elsevier.
40. Le Moullac, G., Quéau, I., Souchu, P. L., Pouvreau, S., Moal, J., Coz, J. R. L. and Samain, J. F. (2007a). Metabolic adjustments in the oyster Crassostrea gigas according to oxygen level and temperature. Mar. Biol. Res. 3, 357-366.
41. Le Moullac, G., Bacca, H., Huvet, A., Moal, J., Pouvreau, S. and Van Wormhoudt, A. (2007b). Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia. J. Exp. Zool. A. 307, 371-382.
42. Leary, S. C., Lyons, C. N., Rosenberger, A. G., Ballantyne, J. S., Stillman, J. and Moyes, C. D. (2003). Fiber-type differences in muscle mitochondrial profiles. Am. J. Physiol. 285, R817-R826.
43. Massabuau, J.-C. (2001). From low arterial-to low tissue-oxygenation strategy. An evolutionary theory. Respir. Physiol. 128, 249-261.
44. McDonald, A. E. and Vanlerberghe, G. C. (2004). Branched mitochondrial electron transport in the Animalia: presence of alternative oxidase in several animal phyla. IUBMB Life 56, 333-341.
45. McDonald, A. E., Vanlerberghe, G. C. and Staples, J. F. (2009). Alternative oxidase in animals: unique characteristics and taxonomic distribution. J. Exp. Biol. 212, 2627-2634.
46. Njogu, R. M., Whittaker, C. J. and Hill, G. C. (1980). Evidence for a branched electron transport chain in Trypanosoma brucei. Mol. Biochem. Parasitol. 1, 13-29.
47. Pichaud, N., Rioux, P. and Blier, P. U. (2012). In situ quantification of mitochondrial respiration in permeabilized fibers of a marine invertebrate with low aerobic capacity. Comp. Biochem. Physiol. 161A, 429-435.
48. Pichavant, K., Person-Le-Ruyet, J., Le Bayon, N., Sévère, A., Le Roux, A., Quéméner, L., Maxime, V., Nonnotte, G. and Boeuf, G. (2000). Effects of hypoxia on growth and metabolism of juvenile turbot. Aquaculture 188, 103-114.
49. 2 (s) in oxyconforming and oxyregulating animals: gas exchange, metabolic rate and the mode of energy production. In The Vertebrate Gas Transport Cascade - Adaptations to Environment and Mode of Life (ed. J. Eduardo and P. W. Bicudo), pp. 330-357. Boca Raton, FL: CRC Press.
50. Schumacker, P. T., Chandel, N. and Agusti, A. G. (1993). Oxygen conformance of cellular respiration in hepatocytes. Am. J. Physiol. 265, L395-L402.
51. Sidell, B. D. (1983). Cellular acclimatisation to environmental change by quantitative alterations in enzymes and organelles. In Cellular Acclimatisation to Environmental Change (ed. A. R. Cossins and P. Sheterline), pp. 103-120. London: Cambridge University Press.
52. Sokolova, I. M. and Sokolov, E. P. (2005). Evolution of mitochondrial uncoupling proteins: novel invertebrate UCP homologues suggest early evolutionary divergence of the UCP family. FEBS Lett. 579, 313-317.
53. St-Pierre, J., Brand, M. D. and Boutilier, R. G. (2000a). The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs. J. Exp. Biol. 203, 1469-1476.
54. St-Pierre, J., Tattersall, G. J. and Boutilier, R. G. (2000b). Metabolic depression and enhanced O2 affinity of mitochondria in hypoxic hypometabolism. Am. J. Physiol. 279, R1205-R1214.
55. Ståhlberg, A., Aman, P., Ridell, B., Mostad, P. and Kubista, M. (2003). Quantitative real-time PCR method for detection of B-lymphocyte monoclonality by comparison of κ and λ immunoglobulin light chain expression. Clin. Chem. 49, 51-59.
56. Storey, K. B. (1996). Oxidative stress: animal adaptations in nature. Braz. J. Med. Biol. Res. 29, 1715-1733.
57. Stuart, J. A., Gillis, T. E. and Ballantyne, J. S. (1998). Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails. Am. J. Physiol. 275, R1977-R1982.
58. Sussarellu, R., Fabioux, C., Le Moullac, G., Fleury, E. and Moraga, D. (2010). Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar. Genomics 3, 133-143.
59. Sussarellu, R., Fabioux, C., Camacho Sanchez, M., Le Goïc, N., Lambert, C., Soudant, P. and Moraga, D. (2012). Molecular and cellular response to short-term oxygen variations in the Pacific oyster Crassostrea gigas. J. Exp. Mar. Biol. Ecol. 412, 87-95.
60. Tschischka, K., Abele, D. and Pörtner, H. O. (2000). Mitochondrial oxyconformity and cold adaptation in the polychaete Nereis pelagica and the bivalve Arctica islandica from the Baltic and White Seas. J. Exp. Biol. 203, 3355-3368.
61. Turrens, J. F. (2003). Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335-344.
62. Vanlerberghe, G. C. and McIntosh, L. (1997). Alternative oxidase: from gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 703-734.
63. Williams, J. N., Jr (1964). A method for the simultaneous quantitative estimation of cytochromes a, b, c1, and c in mitochondria. Arch. Biochem. Biophys. 107, 537-543.
64. Wu, R. S. S. (2002). Hypoxia: from molecular responses to ecosystem responses. Mar. Pollut. Bull. 45, 35-45.