Review and perspectives of physiological mechanisms underlying genetically-based resistance of the Pacific oyster Crassostrea gigas to summer mortality

Aquatic Living Resources

Volumn 24, Issue 3, 2011, Pages 227-236

  Samain, Jean François ^a  

^a IFREMER   (France)

Author keywords

Antibacterial activity; Crassostrea gigas; Environmental stress; Host defence; Immunity

Indexed keywords

ANTHROPOGENIC EFFECT; ANTIMICROBIAL ACTIVITY; CONCEPTUAL FRAMEWORK; DISEASE RESISTANCE; ENDOCRINE DISRUPTOR; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; IMMUNITY; LITERATURE REVIEW; MORALITY; MORTALITY; OYSTER CULTURE; PATHOLOGY; PHYSIOLOGY; RESEARCH WORK; SUMMER; TEMPERATURE EFFECT;

CRASSOSTREA GIGAS; INVERTEBRATA; ONCORHYNCHUS; OSTREIDAE; VERTEBRATA;

EID: 80155210219     PISSN: 09907440     EISSN: 17652952     Source Type: Journal    
DOI: 10.1051/alr/2011144     Document Type: Article

References (78)

1. Abele D., Strahl J., Brey T., Philipp E.E.R., 2008, Imperceptible senescence: Ageing in the ocean quahog Arctica islandica. Free Radical Res. 42, 474-480. (Pubitemid 351935161)
2. Allen S.K, Downing S.L., 1986, Performance of triploid Pacific oysters, Crassostrea gigas (Thunberg). I. Survival, growth, glycogen content, and sexual maturation in yearlings. J. Exp. Mar. Biol. Ecol. 102, 197-208.
3. Barja G., 2000, The flux of free radical attack through mitochondrial DNA is related to aging rate. Aging Clin. Exp. Res. 12, 342-355.
4. Bayne B.L., Newell R.C., 1983, Physiological energetics of marine molluscs. In: Wilbur K.M., Saleuddin A.S. (Eds.), The Mollusca, Vol. 4. Academic Press, New York, pp. 407-515
5. Boudry P., Dégremont L., Haffray P., 2008, The genetic basis of summer mortality in Pacific oyster spat and potential for improving survival by selective breeding in France. In: Samain J.F., McCombie H. (Eds.) Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project. Quae, Versailles, pp. 153-196.
6. Buttemer W.A., Abele D., Costantini D., 2010, The ecology of antioxidants and oxidative stress in animals. From bivalves to birds: oxidative stress and longevity. Funct. Ecol. 24, 971-983.
7. da Silva P.M., Fuentes J., Villalba A., 2009, Differences in gametogenic cycle among strains of the European flat oyster Ostrea edulis and relationship between gametogenesis and bonamiosis. Aquaculture 287, 253-265.
8. De Decker S., Normand J., Saulnier D., Pernet F., Castagnet S., Boudry P., 2011, Responses of diploid and triploid Pacific oysters Crassostrea gigas to Vibrio infection in relation to their reproductive status. J. Invertebr. Pathol. 106, 179-19.
9. Dégremont L., 2003, Etude des bases génétiques de la mortalité estivale et des relations avec la croissance chez les juvéniles de l'huître creuse Crassostrea gigas. Thèse Doctorat Univ. Caen.
10. Dégremont L., Ernande B., Bedier E., Boudry, P., 2007, Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). I. Estimation of genetic parameters for survival and growth. Aquaculture 262, 41-53. (Pubitemid 46137942)
11. Delaporte M., Soudant P., Lambert C., Jegaden M., Moal J., Pouvreau S., Degremont L., Boudry P., Samain J.F., 2007, Characterisation of physiological and immunological differences between Pacific oysters (Crassostrea gigas) genetically selected for high or low survival to summer mortalities and fed different rations under controlled conditions. J. Exp. Mar. Biol. Ecol. 353, 45-57. (Pubitemid 350054946)
12. Duchemin M.B., Fournier M., Auffret M., 2006, Seasonal variations of immune parameters in diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg). Aquaculture 264, 73-81.
13. Duperthuy M., Schmitt P., Garzon E., Caro A., Rosa R.D., Le Roux F., Lautredou-Audouy N., Got P., Romestand B., de Lorgeril J., Kieffer-Jaquinod S., Bachère E., Destoumieux-Garzon D., 2011, Use of OmpU porins for attachment and invasion of Crassostrea gigas immune cells by the oyster pathogen Vibrio splendidus. Proc. Nat. Acad. USA 108, 2993-2998.
14. Fabioux C., Corporeau C., Quillien V., Favrel P., Huvet A., 2009, In vivo RNA interference in oyster vasa silencing inhibits germ cell development. FEBS J. 276, 2566-2573.
15. Fabioux C., Pouvreau S., Le Roux F., Huvet A., 2004, The oyster vasa-like gene: a specific marker of the germ line in Crassostrea gigas. Biochem. Biophys. Res. Comm. 315, 897-904. (Pubitemid 38249388)
16. Fleury E., Fabioux C., Lelong C., Favrel P., Huvet A., 2008, Characterization of a gonad-specific transforming growth factor-beta superfamily member differentially expressed during the reproductive cycle of the oyster Crassostrea gigas. Gene 410, 187-196.
17. Fleury E., Huvet A., Lelong C., de Lorgeril J., Boulo V., Gueguen Y., Bachère E., Tanguy A., Moraga D., Fabioux C., Lindeque P., Shaw J., Reinhardt R., Prunet P., Davey G., Lapegue S., Sauvage C., Corporeau C., Moal J., Gavory F., Wincker P., Moreews F., Klopp C., Mathieu M., Boudry P., Favrel P., 2009, Generation and analysis of a 29 745 unique expressed sequence tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the Gigas Database. BMC Genomics 10, 341.
18. Fleury E., Moal J., Boulo V., Daniel J.Y., Mazurais D., Hénaut A., Corporeau C., Boudry P., Favrel P., Huvet A., 2010, Microarray-based identification of gonad transcripts differentially expressed between lines of Pacific oyster selected to be resistant or susceptible to summer mortality. Mar. Biotechnol. 12, 326-339.
19. Fleury E., Huvet A., 2011, Microarray analysis highlights immune response of Pacific oysters as a determinant of resistance to summer mortality syndrome. Mar. Biotechnol. in press DOI: 10.1007/s10126-011-9403-6.
20. Franco A., Kellner K., Mathieu M., Lelong C., Goux D., Heude- Berthelin C., 2011, Male germ cells of the Pacific oyster Crassostrea gigas: flow cytometry analysis, cell sorting and molecular expression. Aquat.Living Resour. 24.
21. Gabitta S.P., Butterfield D.A., Hensley K., Shaw W., Carney J.M., 1997, Aging and caloric restriction affect mitochondrial respiration and lipid membrane status: an electron paramagnetic resonance investigation. Free Radic. Biol. Med. 23, 191-201. (Pubitemid 27280491)
22. Gaikwad A., Biju K.C., Saha S.G., Subhedar N., 2004, Neuropeptide Y in the olfactory system, forebrain and pituitary of the teleost, Clarias batrachus. J. Chem. Neuroanat. 27, 55-70. (Pubitemid 38230832)
23. Gagnaire B., Soletchnik P., Madec P., Geairon P., Le Moine O., Renault T., 2006, Diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg), reared at two heights above sediment in Marennes-Oleron Basin, France: difference in mortality, sexual maturation and hemocyte parameters. Aquaculture 254, 606-616.
24. Gonzalez M., Gueguen Y., Desserre G., de Lorgeril J., Romestand B., Bachère E., 2007, Molecular characterization of two isoforms of defensin from hemocytes of the oyster Crassostrea gigas. Dev. Comp. Immunol. 31, 332-339. (Pubitemid 44940903)
25. Grangere K., Menesguen A., Lefebvre S., Bacher C., Pouvreau S., 2009, Modelling the influence of environmental factors on the physiological status of the Pacific oyster Crassostrea gigas in an estuarine embayment; The Baie des Veys (France). J. Sea Res. 62 Special Issue, 147-158.
26. Guderley H., Brokordt K., Pérez Cortés H.M., Marty Y., Kraffe E., 2011, Diet and performance in the scallop, Argopecten purpuratus: force production during escape responses and mitochondrial oxidative capacities. Aquat.Living Resour. 24, 3.
27. Gueguen Y., Bernard B., Fievet J., Schmitt P., Destoumieux-Garzón D., Vandenbulcke F., Bulet P., Bachère E., 2009, Oyster hemocytes express a proline-rich peptide displaying synergistic antimicrobial activity with a defensin. Mol. Immunol. 46, 516-522.
28. Gueguen Y., Cadoret J.P., Flament D., Barreau-Roumiguière C., Girardot A.L., Garnier J., Hoareau A., Bachère E., Escoubas J.M., 2003, Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster Crassostrea gigas. Gene 303, 139-145. (Pubitemid 36151778)
29. Guo X., DeBrosse G.A., Allen S.K., 1996, All-triploid Pacific oysters (Crassostrea gigas Thunberg) produced by mating tetraploids and diploids. Aquaculture 149-161. (Pubitemid 126653455)
30. Handley S.J., 1997, Optimizing subdital oyster production, Marlborough Sounds, New Zealand: spionid polychaete infestations, water depth and spat stunting. J. Shellfish Res. 16, 143-150. (Pubitemid 27358169)
31. Heininger K., 1999, A unifiying hypothesis of Alzheimer's disease. I. Ageing sets the stage. Hum. Psychopharmacol. Clin. Exp. 14, 363-414.
32. Heininger K., 2001, The deprivation syndrome is the driving force of phylogeny, ontogeny and oncogeny. Rev. Neurosci. 12, 217-287. (Pubitemid 32843506)
33. Heininger K., 2002, Aging is a deprivation syndrome driven by a germ-soma conflict. Ageing Res. Rev. 1, 481-536. (Pubitemid 38340336)
34. Hewes R.S., Taghert P.H., 2001, Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res. 11, 1126-1142. (Pubitemid 32834556)
35. Hosono R., Nishimoto S., Kuno S., 1989, Alteration of life span in the nematode Caenorhabditis elegans under monoxenic culture conditions. Exp. Gerontol. 24, 251-264. (Pubitemid 19154170)
36. Huvet A., Normand J., Fleury E., Quillien V., Fabioux C., Boudry P., 2010, Reproductive effort of Pacific oysters: a trait associated with susceptibility to summer mortality. Aquaculture 304, 95-99.
37. Huvet A., Royer J., Moal J., Burgeot T., Lapègue S., Boulo V., Nicolas J.L., Lambert C., Van Wormhoudt A., Samain J.F., 2008, Phenotypic characteristics of "R" and "S" oysters lines, selected for resistance or susceptibility to summer mortality In: Samain J.F., McCombie H. (Eds.), Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project, Quae, Versailles, pp. 197-241.
38. Jeschke J.M., Gabriel W., Kokko H., 2008, r-Strategist/K-Strategists. In: Jørgensen S.E., Fath B.D. (Eds.). Encyclopedia of Ecology, pp. 3113-3122.
39. Jiang H., Ren F., Sun J., He L., Li W., 2010, Molecular cloning and gene expression analysis of the leptin receptor in the Chinese mitten crab Eriocheir sinensis. PLoSone 5(6), e11175. doi: 10.1371/journal.pone.0011175.
40. Johnson R.M., Johnson T.M., Londraville R.L., 2000, Evidence for leptin expression in fishes. J. Exp. Zool. 286, 718-724. (Pubitemid 30308323)
41. de Jong-Brink M., 2001, NPY in invertebrates: molecular answers to altered functions during evolution. Peptides 22, 309-315. (Pubitemid 32250230)
42. Jouaux A., Heude-Berthelin C., Sourdaine P., Mathieu M., Kellner K., 2010, Gametogenic stages in triploid oysters Crassostrea gigas: J. Exp. Mar. Biol. Ecol. 395, 162-170.
43. Katayama K., Ikeda Z., Shinohara M., 1979, The growth and survival of the seed oyster Crassostrea gigas with different hardening effects. Bull. Fish. Exp. Stn. Okayama Prefect., pp. 176-180.
44. Kiris I., Eroldogan O., Kir M., Kumlu M., 2004, Influence of neuropeptide Y (NPY) on food intake and growth of penaeid shrimps and Marsupenaeus japonicus and Paneaus semisulcatus (Decapoda: Penaeidae). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 139, 239-244. (Pubitemid 39445372)
45. Kirkwood T.B.L., Kowald A., 1997, Network theory of aging. Exp. Gerontol. 32, 395-399. (Pubitemid 27366478)
46. Kooijman S.A.L.M., 2000, Dynamic energy and mass budgets in biological systems. Cambridge University Press, Cambridge, UK.
47. Kuzmin E.V., Karpora O.V., Elthon T.E., Newton K.J., 2004, Mitochondrial respiratory deficiencies signal up-regulation of genes of heat shock proteins. J. Biol. Chem. 279, 20672-20677. (Pubitemid 38656462)
48. Lambert C., Moal J., Le Moullac, Pouvreau S., 2008, Mortality risks associated with physiological traits of oysters during reproduction. In: Samain J.F., McCombie H. (Eds.), Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project, Quae, Versailles, pp. 63-106.
49. Larsson T.A., Larson E.T., Fredriksson R., Conlon J.M., Larhammar D., 2006, Characterization of NPY receptor subtypes Y2 and Y7 in rainbow trout Oncorhynchus mykiss. Peptides 27, 1320-1327. (Pubitemid 43767007)
50. Lin S.J., Defossez P.A., Guarente L., 2000, Requirements of NAD and SIR2 for life span extension by caloric restriction in Saccharomyces cerevisiae. Science 289, 2126-2128.
51. MacArthur R.H., Wilson E.O., 1967, The theory of island biogeography. Princeton University Press, Princeton.
52. Masoro E.J., 1998, Influence of caloric intake on aging and on the response to stressors. J. Toxicol. Environ. Health. Part B, 1, Crit. Rev. 1, 243-257. (Pubitemid 128693560)
53. Mateo D.R., Greenwood S.J., Araya M.T., Berthe F.C.J., Johnson G.R., Siah A., 2010, Differential gene expression of gamma-actin, Toll-like receptor 2 (TLR-2) and interleukin-1 receptor-associated kinase 4 (IRAK-4) in Mya arenaria haemocytes induced by in vivo infections with two Vibrio splendidus strains. Dev. Comp. Immunol. 34, 710-714.
54. Mori K., 1979, Effects of artificial eutrophication on the metabolism of the Japanese oyster Crassostrea gigas. Mar. Biol. 53, 361-369
55. Na G.H., Lee C.S., Choi W.J., 1991, The effect of dissolved oxygen on the estival mass mortality of sea squirt Halocynthia roretzi. Bull. Korean Fish. Soc. 24, 52-58.
56. Pouvreau S., Bourlès Y., Lefèbvre S., Gangnery A., Alunno-Bruscia M., 2006, Application of a dynamic energy budget model to the Pacific oyster, Crassostrea gigas, reared under various environmental conditions. J. Sea Res. 56, 156-167. (Pubitemid 44316934)
57. Rao G., Xia E., Nadakavukaren M.J., Richardson A., 1990, Effect of dietary restriction on the age-dependent changes in the expression of antioxidant enzymes in rat liver. J. Nutr. 120, 602-609. (Pubitemid 20197966)
58. Renault T., Faury N., Barbosa-Solomieu V., Moreau K., 2011, Suppression substractive hybridisation (SSH) and real time PCR reveal differential gene expression in the Pacific cupped oyster, Crassostrea gigas, challenged with Ostreid herpesvirus 1. Dev. Comp. Immunol. 35, 725-735.
59. Risby T.H., Jiang L., Stoll S., Ingram D., Spankler E., Heim J., Cutler R., Roth G.S., Rifkind J.M., 1999, breath ethane as a marker of reactive oxygen species during manipulation of diet and oxygen tension in rats. J. Appl. Physiol. 86, 617-622. (Pubitemid 29075816)
60. Samain J.F., Dégremont L., Soletchnik P., Haure J., Bédier E., Ropert M., Moal J., Huvet A., Bacca H., Van Wormhoudt A., Delaporte M., Costil K., Pouvreau S., Lambert C., Boulo V., Soudant P., Nicolas J.L., Le Roux F., Renault T., Gagnaire B., Geret F., Boutet I., Burgeot T., Boudry P., 2007, Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes. Aquaculture 268, 227-243. (Pubitemid 47023090)
61. Samain J.F., McCombie, H., 2008, Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project. Quae, Versailles.
62. Samain J.F., Ropert M., Bédier E., Soletchnik P., Mazurié J., Le Coz F., Blin J.L., Costil K., Mille D., Trintignac P., Boudry P., Haffray P., Bacher C., Grangeré K., Pouvreau S., Bourles Y., Sylvand B., Misko P., Gohin F., Woerther P., 2008, A synthesis of the Morest project and recommendations for forecasting and managing oyster summer mortalities. In: Samain, J.F., McCombie H. (Eds.), Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project, Quae, Versailles, pp. 307-348.
63. Saraiva S., van der Meer J., Kooijman S.A.L.M., Sousa T., 2011, Modelling feeding processes in bivalves: a mechanistic approach. Ecol. Model. 222, 514-523.
64. Schneider J.E., 2004, Energy balance and reproduction. Physiol. Behav. 81, 289-317. (Pubitemid 38670092)
65. Segarra A., Pépin J.F., Arzul I., Morga B., Faury N., Renault T., 2010, Detection and description of a particular Ostreid herpes virus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res. 153, 92-99.
66. Singru P.S., Mazumdar M., Barsagade V., Lechan R.M., Thim L., Clausen J.T., Subhedar N., 2008, Association of cocaine- and amphetamine-regulated transcript and neuropeptide Y in the forebrain and pituitary of the catfish, Clarias batrachus: a double immuno fluorescentlabeling study. J. Chem. Neuroanat. 36, 239-50.
67. Sohal R.S., Weindruch R., 1996, Oxidative stress, caloric restriction, and aging. Science 273, 59-63. (Pubitemid 26255420)
68. Strahl J., Abele D., 2010, Cell turnover in tissues of the long-lived ocean quahog Arctica islandica and the short-lived scallop Aequipecten opercularis. Mar. Biol. 157, 1283-1292.
69. Sussarellu R., Fabioux C., Le Moullac G., Fleury E., Moraga D., 2010, Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar. Genom. 3, 133-143.
70. Tensen C.P., Cox K.J., Burke J.F., Leurs R., van der Schors R.C., Geraerts W.P., Vreugdenhil E., Heerikhuizen H., 1998, Molecular cloning and characterization of an invertebrate homologue of a neuropeptide Y receptor. Eur. J. Neurosci. 10, 3409-3416. (Pubitemid 29074132)
71. Terashima S., Katayama K., Shinohara M., Ikeda Z., 1978, Hardening methods of the seed oyster, Crassostrea gigas for the culture of the oyster. Bull. Fish. Exp. Stn. Okayama Prefect. 3, 150-156.
72. Travers M.A., Le Goïc N., Huchette S., Koken M., Paillard C., 2008, Summer immune depression associated with increased susceptibility of the European abalone, Haliotis tuberculata to Vibrio harveyi infection. Fish Shellfish Immunol. 25, 800-808.
73. Unniappan S., Peter R.E., 2005, Structure, distribution and physiological functions of ghrelin in fish. Comp. Biochem.Physiol. Part A Mol. Integr. Physiol. 140, 396-408. (Pubitemid 40779983)
74. Wanagat J., Weindruch R., 2000, Caloric restriction and aging: studies in rodent and primates. In: Morley J.E., Armbrecht H.T., Coe R.M., Vellas B. (Eds.), The sciences of geriatrics. Serdi Publisher, Paris, pp. 153-165.
75. Warren C.E., Davis G.E., 1967, Laboratory studies on the feeding, bioenergetics and growth of fishes. In: Gerking S.D. (Ed.), The Biological Basis of Freshwater Fish Production. Blackwell Scientific Publications, Oxford, pp. 175-214.
76. Weindruch R., Walford R.L., 1988, The retardation of aging and disease by dietary restriction. Thomas C.C. (Ed.) Springfield IL.
77. Widdows J., Johnson D., 1988, Physiological energetics of Mytilus edulis: scope for growth. Mar. Ecol. Prog. Ser. 46, 113-12.
78. Xiao J., Ford S.E., Yang H., Zhang G., Zhang F., Guo X., 2005, Studies on mass summer mortality of cultured zhikong scallops (Chlamys farreri Jones et Preston) in China. Aquaculture 250, 602-615. (Pubitemid 41727972)