Anaerobic metabolic patterns related to stress responses in hypoxia exposed mussels Mytilus galloprovincialis

Journal of Experimental Marine Biology and Ecology

Volumn 394, Issue 1-2, 2010, Pages 123-133

  Anestis, Andreas ^a   Pörtner, Hans O ^b   Michaelidis, Basile ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

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

Author keywords

Bivalves; Exposure to air; Hsps; Mortality; PK; Thermal limits

Indexed keywords

AIR EXPOSURE; ANOXIC CONDITIONS; BIVALVE; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; HEAT SHOCK; HYPOXIA; METABOLISM; MORTALITY; PROTEIN; TEMPERATURE EFFECT;

BIVALVIA; MYTILUS GALLOPROVINCIALIS;

EID: 77956741714     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2010.08.008     Document Type: Article

References (70)

1. Airaksinen S., Rabergh C.M.I., Sistonen L., Nikinmaa M. Effects of heat shock and hypoxia on protein synthesis in rainbow trout (Oncorhynchus mykiss) cells. J. Exp. Biol. 1998, 201:2543-2551.
2. Anestis A., Lazou A., Pörtner H.O., Michaelidis B. Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am. J. Physiol.-Reg. Integr. Comp. Physiol. 2007, 293:R911-R921.
3. Anestis A., Pörtner H.O., Lazou A., Michaelidis B. Metabolic and molecular stress responses of sublittoral bearded horse mussel Modiolus barbatus to warming sea water. Implications for vertical zonation. J. Exp. Biol. 2008, 211:2889-2898.
4. Babarro J.M.F., Labarta U., Reiriz F.M.J. Energy metabolism and performance of Mytilus galloprovincialis under anaerobiosis. J. Mar. Biol. Assoc. U.K. 2007, 87:941-946.
5. Beckmann R.P., Lovett M., Welch W.J. Examining the function and regulation of hsp70 in cells subjected to metabolic stress. J. Cell Biol. 1992, 117:1137-1150.
6. Benjamin I.J., Horie S., Greenberg M.L., Alpern R.J., Williams R.S. Induction of stress proteins in cultured myogenic cells. Molecular signals for the activation of heat shock transcription factor during ischemia. J. Clin. Invest. 1992, 89:1685-1689.
7. Brooks S.P.J., Storey K.B. Glycolytic controls in estivation and anoxia: A comparison of metabolic arrest in land and marine molluscs. Comp. Biochem. Physiol. A. 1997, 118:1103-1114.
8. Buck L.T., Hochachka P.W. Anoxia-tolerant hepatocytes-Model system for study of reversible metabolic suppression. Am. J. Phys. 1993, 265:R49-R56.
9. Buckley B.A., Owen M.E., Hofmann G.E. Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J. Exp. Biol. 2001, 204:2816-2829.
10. David E., Tanguy A., Pichavant K., Moraga D. Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J. 2005, 272:5635-5652.
11. De Vooys C.G.N. Anaerobic metabolism in sublittoral living Mytilus galloprovincialis in the Mediterranean. 1. Partial adaptation of anaerobic energy-metabolism. Neth. J. Sea Res. 1979, 13(2):192-202.
12. De Zwaan A., Richard H.M.E. Anoxic or aerial survival of bivalves and other euryoxic invertebrates as a useful response to environmental stress-A comprehensive review. Comp. Biochem. Physiol. 1996, 113C:299-312.
13. De Zwaan A., Cortesi P., Van Den Thillart G., Roos J., Storey K.B. Differential sensitivities to hypoxia by two anoxia-tolerant marine molluscs: A biochemical analysis. Mar. Biol. 1991, 111:343-351.
14. De Zwaan A., Cortesi P., van den Thillart G., Brooks S., Storey K.B., Roos J., Van Lieshout G., Cattani O., Vitali G. Energy metabolism of bivalves at reduced oxygen tensions. Marine coastal eutrophication 1992, 1029-1039. Elsevier, Amsterdam. R.A. Vollenweider, R. Marchetti, R. Viviani (Eds.).
15. Delaney M.A., Klesius P.H. Hypoxic conditions induce Hsp70 production in blood, brain and head kidney of juvenile Nile tilapia Oreochromis niloticus (L.). Aquaculture 2004, 236:633-644.
16. Diaz-Enrich M.J., Ramos-Martinez I.J., Ibarguren I. Implication of guanosine 3′, 5′-cyclic monophosphate, adenosine 3′, 5′-cyclic monophosphate, adenosine 5′-mono-, di- and triphosphate and fructose-2, 6-bisphosphate in the regulation of the glycolytic pathway in hypoxic/anoxic mussel, Mytilus galloprovincialis. Mol. Cell. Biochem. 2002, 240:111-118.
17. Gaitanaki C., Kefaloyianni E., Marmari A., Beis I. Various stressors rapidly activate the p38-MAPK signaling pathway in Mytilus galloprovincialis (Lam.). Mol. Cell. Biochem. 2004, 260:119-127.
18. Gilman S.E., Wethey D.S., Helmuth B. Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales. PNAS 2006, 103:9560-9565.
19. Gonzalez M., Lowenstein D., Fernyak S., Hisanaga K., Simon R., Sharp F. Induction of Heat Shock Protein 72 like immunoreactivity in the hippocampal formation following transient global ischemia. Brain Res. Bull. 1991, 26:241-250.
20. Gourgou E., Aggeli I.-K., Beis I., Gaitanaki C. Hyperthermia-induced Hsp70 and MT20 transcriptional upregulation are mediated by p38-MAPK and JNKs in Mytilus galloprovincialis (Lamarck); a pro-survival response. J. Exp. Biol. 2010, 213:347-357.
21. Grieshaber M.K., Hardewig I., Kreutzer U., Pörtner H.O. Physiological and metabolic responses to hypoxia in invertebrates. Rev. Physiol. Biochem. Pharmacol. 1994, 125:43-147.
22. Hayward S.A.L., Rinehart J.P., Denlinger D.L. Desiccation and rehydration elicit distinct heat shock protein transcript responses in flesh fly pupae. J. Exp. Biol. 2004, 207(6):963-971.
23. Hayward S.A.L., Pavlides S.C., Tammariello S.P., Rinehart J.P., Denlinger D.L. Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. J. Insect Physiol. 2005, 51(6):631-640.
24. Helmerhorst E., Strokes B.G. Microcentrifuge desalting: a rapid quantitative method for desalting small amounts of protein. Anal. Biochem. 1980, 104:130-135.
25. Helmuth B.S.T. Intertidal mussel microclimates: predicting the body temperature of a sessile invertebrate. Ecol. Monogr. 1998, 68:51-74.
26. Helmuth B. How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics. Integr. Comp. Biol. 2002, 42:837-845.
27. Helmuth B. From cells to coastlines: How can we use physiology to forecast the impacts of climate change?. J. Exp. Biol. 2009, 212:753-760.
28. Helmuth B., Harley C.D.G., Halpin P.M., O'Donnell M., Hofmann G.E., Blanchette C.A. Climate change and latitudinal patterns of intertidal thermal stress. Science 2002, 298:1015-1017.
29. Helmuth B., Broitman B.R., Blanchette C.A., Gilman S., Halpin P., Harley C.D.G., O' Donnell M.J., Hofmann G.E., Menge B., Strickland D. Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change. Ecol. Monogr. 2006, 76(4):461-479.
30. Hochachka P.W., Buck L.T., Doll C.J., Land S.C. Unifying theory of hypoxia tolerance: molecular / metabolic defence and rescue mechanisms for surviving oxygen lack. Biochemistry 1996, 93:9493-9498.
31. Hofmann G.E. Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am. Zool. 1999, 39:889-900.
32. Hofmann G.E., Somero G.N. Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal mussel Mytilus trossulus. J. Exp. Biol. 1995, 198:1509-1518.
33. Hofmann G.E., Somero G.N. Interspecific variation in thermal denaturation of proteins in the congeneric mussels Mytilus trossulus and M. galloprovincialis: Evidence from the heat shock response and protein ubiquitination. Mar. Biol. 1996, 126:65-75.
34. Hofmann G.E., Todgham A.E. Living in the now: Physiological mechanisms to tolerate a rapidly changing environment. Annu. Rev. Physiol. 2010, 72:22.1-22.19.
35. Holm K., Hernroth B., Thorndyke M. Coelomocyte numbers and expression of Hsp70 in wounded sea stars during hypoxia. Cell Tissue Res. 2008, 334:319-325.
36. Isani G., Cattani O., Zurzolo M., Pagnucco C., Cortesi P. Energy metabolism of the mussel, Mytilus galloprovincialis, during long-term anoxia. Comp. Biochem. Physiol. 1995, 110B:103-113.
37. Kassahn K.S., Crozier R.H., Portner H.O., Caley M.J. Animal performance and stress: responses and tolerance limits at different levels of biological organisation. Biol. Rev. 2009, 84:277-292.
38. Kefaloyianni E., Gourgou E., Ferle V., Kotsakis E., Gaitanaki C., Beis I. Acute thermal stress and various heavy metals induce tissue-specific pro- or antiapoptotic events via the p38-MAPK signal transduction pathway in Mytilus galloprovincialis (Lam.). J. Exp. Biol. 2005, 208:4427-4436.
39. Kleger C.K. Heat shock proteins: Modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 2002, 92:2177-2186.
40. Kluytmans J.H., De Bont A.M.T., Kruitwagen E.C.J., Revestein H.J.L., Veenhof P.R. Anaerobic capacities and anaerobic energy production of some mediterranean bibalves. Comp. Biochem. Physiol. 1983, 75B:171-179.
41. Knowlton A.A., Brecher P., Apstein C.S. Rapid expression of heat shock protein in the rabbit after brief cardiac ischemia. J. Clin. Invest. 1991, 87:139-147.
42. Land S.C., Hochachka P.W. A heme-protein-based oxygen-sensing mechanism controls the expression and suppression of multiple proteins in anoxia-tolerant turtle hepatocytes. PANAS 1995, 92:7505-7509.
43. LeBlanc N., Landry T., Stryhn H., Tremblay R., McNiven M., Davidson J. The effect of high air and water temperature on juvenile Mytilus edulis in Prince Edward Island, Canada. Aquaculture 2005, 243(1-4):185-194.
44. MacRae T.H. Molecular chaperones, stress resistance and development in Artemia franciscana. Semin. Cell Dev. Biol. 2003, 14(5):251-258.
45. 31P-MRS. Am. J. Physiol. 2002, 283(5):R1254-R1262.
46. Matranga V., Toia G., Bonaventura R., Müller W.E.G. Cellular and biochemical responses to environmental and experimentally induced stress in sea urchin coelomocytes. Cell Stress Chap. 2000, 5:113-120.
47. Michaelidis B., Haas D., Grieshaber K.M. Extracellular and intracellular acid-base status with regard to energy metabolism in the oyster Crassostrea gigas during exposure to air. Physiol. Biochem. Zool. 2005, 78:373-383.
48. Mosser D.D., Kotzbauer P.T., Sarge K.D., Morimoto R.I. In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation. Proc. Natl Acad. Sci. USA 1990, 87:3748-3752.
49. Newell R.C. Biology of intertidal animals 1979, Marine Ecological Surveys, Faversham, UK. 3rd ed.
50. Pörtner H.O. Contributions of anaerobic metabolism to pH regulation in animal tissues: theory. J. Exp. Biol. 1987, 131:69-87.
51. Pörtner H.O. Anaerobic metabolism and changes in acid-base status: Quantitative interrelationships and pH regulation in the marine worm Sipunculus nudus. J. Exp. Biol. 1987, 131:89-105.
52. Pörtner H.O. Climate change and temperature dependent biogeography: systemic to molecular hierarchies of thermal tolerance in animals. Comp. Biochem. Physiol. 2002, 132A:739-761.
53. Pörtner H.O., Farrell A.P. Physiology and climate change. Science 2008, 322:690-692.
54. Pörtner H.O., Knust R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 2007, 315:95-97.
55. Pörtner H.O., Grieshaber M.K., Heisler N. Anaerobiosis and acid-base status in marine invertebrates-Effect of environmental hypoxia on extracellular and intracellular pH in Sipunculus nudus. J. Comp. Physiol. B-Biochem. Syst. Envir. Physiol. 1984, 155(1):13-20.
56. Prentice H.M., Milton S.L., Scheurle D., Lutz P.L. The upregulation of cognate and inducible heat shock proteins in the anoxic turtle brain. J. Cereb. Blood Flow Metab. 2004, 24(7):826-828.
57. Ramaglia V., Buck L.T. Time-dependent expression of heat shock proteins 70 and 90 in tissues of the anoxic western painted turtle. J. Exp. Biol. 2004, 207(21):3775-3784.
58. Renshaw G.M.C., Warburton J., Girjes A. Oxygen sensors and energy sensors act synergistically to achieve a graded alteration I gene expression: Consequences for assessing the level of neurpoprotection in response to stressors. Front. Biosc. 2004, 9:110-116.
59. Roberts D.A., Hofmann G.E., Somero G.N. Heat-shock protein expression in Mytilus californianus: Acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol. Bull. 1997, 192:309-320.
60. Schneider K.R. Heat stress in the intertidal: Comparing survival and growth of an invasive and native mussel under a variety of thermal conditions. Biol. Bull. 2008, 215:253-264.
61. Somero G.N. Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front. Zool. 2005, 2. (http://www.frontiersinzoology.com/content/2-1/1).
62. Storey K.B. Molecular mechanisms of metabolic arrest in molluscs. Surviving hypoxia: Mechanisms of control and adaptation 1993, 253-269. CRC Press, Boca Raton. P.W. Hochachka, P.L. Lutz, T.J. Sick, M. Rosenthal, G. Thillart (Eds.).
63. Storey K.B., Storey J.M. Putting life on 'pause'-Molecular regulation of hypometabolism. J. Exp. Biol. 2007, 210:1700-1714.
64. Tomanek L. The importance of physiological limits in determining biogeographical range shifts due to global climate change: The heat-shock response. Physiol. Biochem. Zool. 2008, 81(6):709-717.
65. Van Dijk P.L.M., Tesch C., Hardewig I., Pörtner H.O. Physiological disturbances at critically high temperatures. A comparison between stenothermal Antarctic, and eurythermal temperate eelpouts (Zoarcidae). J. Exp. Biol. 1999, 202:3611-3621.
66. Velazquez J.M., Lindquist S. Hsp70: Nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 1984, 36:652-662.
67. Viant M.R., Werner I., Rosenblum E.S., Gantner A.S., Tjeerdema R.S., Johnson M.L. Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiol. Biochem. 2003, 29:159-171.
68. Why S.K.V., Mann A.S., Thulin G., Zhu X.H., Kashgarian M., Siegel N.J. Activation of heat-shock transcription factor by graded reductions in renal ATP, in vivo, in the rat. J. Clin. Invest. 1994, 94:1518-1523.
69. Widdows J., Bayne B.L., Livingstone D.R., Newell R.I.E., Donkin P. Physiological and biochemical responses of bivalve molluscs to exposure to air. Comp. Biochem. Physiol. Physiol. 1979, 62(2):301-308.
70. Willsie J.K., Clegg J.S. Nuclear p26, a small heat shock/alpha-crystallin protein, and its relationship to stress resistance in Artemia franciscana embryos. J. Exp. Biol. 2001, 204(13):2339-2350.