1932

Abstract

Oysters that occupy estuarine and intertidal habitats have well-developed stress tolerance mechanisms to tolerate harsh and dynamically changing environments. In this review, we summarize common pathways and genomic features in oyster that are responsive to environmental stressors such as temperature, salinity, hypoxia, air exposure, pathogens, and anthropogenic pollutions. We first introduce the key genes involved in several pathways, which constitute the molecular basis for adaptation to stress. We use genome analysis to highlight the strong cellular homeostasis system, a unique adaptive characteristic of oysters. Next, we provide a global view of features of the oyster genome that contribute to stress adaptation, including oyster-specific gene expansion, highly inducible expression, and functional divergence. Finally, we review the consequences of interactions between oysters and the environment from ecological and evolutionary perspectives by discussing mass mortality and adaptive divergence among populations and related species of the genus . We conclude with prospects for future study.

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2016-02-15
2024-03-29
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Literature Cited

  1. Guo X. 1.  2009. Use and exchange of genetic resources in molluscan aquaculture. Rev. Aquacult. 1:251–59 [Google Scholar]
  2. Kawabe S, Takada M, Shibuya R, Yokoyama Y. 2.  2010. Biochemical changes in oyster tissues and hemolymph during long-term air exposure. Fish. Sci. 76:841–55 [Google Scholar]
  3. Damiens G, His E, Gnassia-Barelli M, Quiniou F, Romeo M. 3.  2004. Evaluation of biomarkers in oyster larvae in natural and polluted conditions. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 138:121–28 [Google Scholar]
  4. Luna-Acosta A, Bustamante P, Godefroy J, Fruitier-Arnaudin I, Thomas-Guyon H. 4.  2010. Seasonal variation of pollution biomarkers to assess the impact on the health status of juvenile Pacific oysters Crassostrea gigas exposed in situ. Environ. Sci. Pollut. Res. 17:999–1008 [Google Scholar]
  5. Zhang GF, Fang XD, Guo XM, Li L, Luo RB. 5.  et al. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54 [Google Scholar]
  6. Vabulas RM, Raychaudhuri S, Hayer-Hartl M, Hartl FU. 6.  2010. Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb. Perspect. Biol. 2:12a004390 [Google Scholar]
  7. Chen B, Retzlaff M, Roos T, Frydman J. 7.  2011. Cellular strategies of protein quality control. Cold Spring Harb. Perspect. Biol. 3:a004374 [Google Scholar]
  8. Kawabe S, Yokoyama Y. 8.  2011. Novel isoforms of heat shock transcription factor 1 are induced by hypoxia in the Pacific oyster Crassostrea gigas. J. Exp. Zool. A Comp. Exp. Biol. 315A:394–407 [Google Scholar]
  9. Fabbri E, Valbonesi P, Franzellitti S. 9.  2008. HSP expression in bivalves. Invertebr. Surviv. J. 5:135–61 [Google Scholar]
  10. Shamseldin AA, Clegg JS, Friedman CS, Cherr GN, Pillai MC. 10.  1997. Induced thermotolerance in the Pacific oyster, Crassostrea gigas. J. Shellfish Res. 16:487–91 [Google Scholar]
  11. Clegg JS, Uhlinger KR, Jackson SA, Cherr GN, Rifkin E, Friedman CS. 11.  1998. Induced thermotolerance and the heat shock protein-70 family in the Pacific oyster Crassostrea gigas. Mol. Mar. Biol. Biotechnol 7:21–30 [Google Scholar]
  12. Hamdoun AM, Cheney DP, Cherr GN. 12.  2003. Phenotypic plasticity of HSP70 and HSP70 gene expression in the Pacific oyster (Crassostrea gigas): implications for thermal limits and induction of thermal tolerance. Biol. Bull. 205:160–69 [Google Scholar]
  13. Piano A, Asirelli C, Caselli F, Fabbri E. 13.  2002. Hsp70 expression in thermally stressed Ostrea edulis, a commercially important oyster in Europe. Cell Stress Chaperones 7:250–57 [Google Scholar]
  14. Meistertzheim AL, Tanguy A, Moraga D, Thebault MT. 14.  2007. Identification of differentially expressed genes of the Pacific oyster Crassostrea gigas exposed to prolonged thermal stress. FEBS J. 274:6392–402 [Google Scholar]
  15. Farcy E, Voiseux C, Lebel JM, Fievet B. 15.  2009. Transcriptional expression levels of cell stress marker genes in the Pacific oyster Crassostrea gigas exposed to acute thermal stress. Cell Stress Chaperones 14:371–80 [Google Scholar]
  16. Zhang Y, Sun J, Mu H, Li J, Xu F. 16.  et al. 2014. Proteomic basis of stress responses in the gills of the Pacific oyster Crassostrea gigas. J. Proteome Res. 14:1304–17 [Google Scholar]
  17. Zhao XL, Yu H, Kong LF, Li Q. 17.  2012. Transcriptomic responses to salinity stress in the Pacific oyster Crassostrea gigas. PLOS ONE 7:9e46244 [Google Scholar]
  18. Metzger DC, Pratt P, Roberts SB. 18.  2012. Characterizing the effects of heavy metal and Vibrio exposure on Hsp70 expression in Crassostrea gigas gill tissue. J. Shellfish Res. 31:627–30 [Google Scholar]
  19. Schroder M. 19.  2008. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 65:862–94 [Google Scholar]
  20. Ron D, Walter P. 20.  2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8:519–29 [Google Scholar]
  21. Yokoyama Y, Hashimoto H, Kubota S, Kuriyama A, Ogura Y. 21.  et al. 2006. cDNA cloning of Japanese oyster stress protein homologous to the mammalian 78-kDa glucose regulated protein and its induction by heatshock. Fish. Sci. 72:402–9 [Google Scholar]
  22. Niyogi S, Biswas S, Sarker S, Datta AG. 22.  2001. Antioxidant enzymes in brackishwater oyster, Saccostrea cucullata as potential biomarkers of polyaromatic hydrocarbon pollution in Hooghly Estuary (India): seasonality and its consequences. Sci. Total Environ. 281:237–46 [Google Scholar]
  23. Schlenk D, Buhler DR. 23.  1989. Xenobiotic biotransformation in the Pacific oyster (Crassostrea gigas). Comp. Biochem. Physiol. C 94:469–75 [Google Scholar]
  24. Schlenk D, Buhler DR. 24.  1990. The in vitro biotransformation of 2-aminofluorene in the visceral mass of the Pacific oyster, Crassostrea gigas. Xenobiotica 20:563–72 [Google Scholar]
  25. de Toledo-Silva G, Siebert MN, Medeiros ID, Sincero TC, Moraes MO. 25.  et al. 2008. Cloning a new cytochrome P450 isoform (CYP356A1) from oyster Crassostrea gigas. Mar. Environ. Res. 66:15–18 [Google Scholar]
  26. Boutet I, Tanguy A, Moraga D. 26.  2004. Molecular identification and expression of two non-P450 enzymes, monoamine oxidase A and flavin-containing monooxygenase 2, involved in phase I of xenobiotic biotransformation in the Pacific oyster, Crassostrea gigas. Biochim. Biophys. Acta 1679:29–36 [Google Scholar]
  27. Boutet I, Tanguy A, Moraga D. 27.  2004. Response of the Pacific oyster Crassostrea gigas to hydrocarbon contamination under experimental conditions. Gene 329:147–57 [Google Scholar]
  28. Mello DF, de Oliveira ES, Vieira RC, Simoes E, Trevisan R. 28.  et al. 2012. Cellular and transcriptional responses of Crassostrea gigas hemocytes exposed in vitro to brevetoxin (PbTx-2). Mar. Drugs 10:583–97 [Google Scholar]
  29. Boutet I, Tanguy A, Moraga D. 29.  2004. Characterisation and expression of four mRNA sequences encoding glutathione S-transferases pi, mu, omega and sigma classes in the Pacific oyster Crassostrea gigas exposed to hydrocarbons and pesticides. Mar. Biol. 146:53–64 [Google Scholar]
  30. Zanette J, de Almeida EA, da Silva AZ, Guzenski J, Ferreira JF. 30.  et al. 2011. Salinity influences glutathione S-transferase activity and lipid peroxidation responses in the Crassostrea gigas oyster exposed to diesel oil. Sci. Total Environ. 409:1976–83 [Google Scholar]
  31. Deeley RG, Westlake C, Cole SP. 31.  2006. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 86:849–99 [Google Scholar]
  32. Xu YY, Liang JJ, Yang WD, Wang J, Li HY, Liu JS. 32.  2014. Cloning and expression analysis of P-glycoprotein gene in Crassostrea ariakensis. Aquaculture 418:39–47 [Google Scholar]
  33. Kingtong S, Chitramvong Y, Janvilisri T. 33.  2007. ATP-binding cassette multidrug transporters in Indian-rock oyster Saccostrea forskali and their role in the export of an environmental organic pollutant tributyltin. Aquat. Toxicol. 85:124–32 [Google Scholar]
  34. Ivanina AV, Sokolova IM. 34.  2008. Effects of cadmium exposure on expression and activity of P-glycoprotein in eastern oysters, Crassostrea virginica Gmelin. Aquat. Toxicol. 88:19–28 [Google Scholar]
  35. Zanette J, Goldstone JV, Bainy AC, Stegeman JJ. 35.  2010. Identification of CYP genes in Mytilus (mussel) and Crassostrea (oyster) species: first approach to the full complement of cytochrome P450 genes in bivalves. Mar. Environ. Res. 69:Suppl.S1–3 [Google Scholar]
  36. Goldstone JV, Goldstone HM, Morrison AM, Tarrant A, Kern SE. 36.  et al. 2007. Cytochrome P450 1 genes in early deuterostomes (tunicates and sea urchins) and vertebrates (chicken and frog): origin and diversification of the CYP1 gene family. Mol. Biol. Evol. 24:2619–31 [Google Scholar]
  37. Zanette J, Jenny MJ, Goldstone JV, Parente T, Woodin BR. 37.  et al. 2013. Identification and expression of multiple CYP1-like and CYP3-like genes in the bivalve mollusk Mytilus edulis. Aquat. Toxicol. 128–29:101–12 [Google Scholar]
  38. Limon-Pacheco J, Gonsebatt ME. 38.  2009. The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 674:137–47 [Google Scholar]
  39. Jo PG, An KW, Park MS, Choi CY. 39.  2008. mRNA expression of HSP90 and SOD, and physiological responses to thermal and osmotic stress in the Pacific oyster, Crassostrea gigas. Molluscan Res. 28:158–64 [Google Scholar]
  40. Park MS, Jo PG, Choi YK, An KW, Choi CY. 40.  2009. Characterization and mRNA expression of Mn-SOD and physiological responses to stresses in the Pacific oyster Crassostrea gigas. Mar. Biol. Res. 5:451–61 [Google Scholar]
  41. Lushchak VI. 41.  2011. Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 101:13–30 [Google Scholar]
  42. Lang RP, Bayne CJ, Camara MD, Cunningham C, Jenny MJ, Langdon CJ. 42.  2009. Transcriptome profiling of selectively bred Pacific oyster Crassostrea gigas families that differ in tolerance of heat shock. Mar. Biotechnol. 11:650–68 [Google Scholar]
  43. De Zoysa M, Whang I, Lee Y, Lee S, Lee JS, Lee J. 43.  2009. Transcriptional analysis of antioxidant and immune defense genes in disk abalone (Haliotis discus discus) during thermal, low-salinity and hypoxic stress. Comp. Biochem. Phys. B 154:387–95 [Google Scholar]
  44. Sussarellu R, Fabioux C, Le Moullac G, Fleury E, Moraga D. 44.  2010. Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar. Genomics 3:133–43 [Google Scholar]
  45. Boyd JN, Burnett LE. 45.  1999. Reactive oxygen intermediate production by oyster hemocytes exposed to hypoxia. J. Exp. Biol. 202:3135–43 [Google Scholar]
  46. Meng J, Zhu QH, Zhang LL, Li CY, Li L. 46.  et al. 2013. Genome and transcriptome analyses provide insight into the euryhaline adaptation mechanism of Crassostrea gigas. PLOS ONE 8:3e58563 [Google Scholar]
  47. Funes V, Alhama J, Navas JI, López-Barea J, Peinado J. 47.  2006. Ecotoxicological effects of metal pollution in two mollusc species from the Spanish South Atlantic littoral. Environ. Pollut. 139:214–23 [Google Scholar]
  48. Jo PG, Choi YK, Choi CY. 48.  2008. Cloning and mRNA expression of antioxidant enzymes in the Pacific oyster, Crassostrea gigas in response to cadmium exposure. Comp. Biochem. Phys. C 147:460–69 [Google Scholar]
  49. Kerr JF, Wyllie AH, Currie AR. 49.  1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239–57 [Google Scholar]
  50. Meier P, Finch A, Evan G. 50.  2000. Apoptosis in development. Nature 407:796–801 [Google Scholar]
  51. Qu T, Huang B, Zhang L, Li L, Xu F. 51.  et al. 2014. Identification and functional characterization of two executioner caspases in Crassostrea gigas. PLOS ONE 9:e89040 [Google Scholar]
  52. Qu T, Zhang L, Wang W, Huang B, Li Y. 52.  et al. 2015. Characterization of an inhibitor of apoptosis protein in Crassostrea gigas clarifies its role in apoptosis and immune defense. Dev. Comp. Immunol. 51:74–78 [Google Scholar]
  53. Zhang L, Li L, Zhang G. 53.  2011. Gene discovery, comparative analysis and expression profile reveal the complexity of the Crassostrea gigas apoptosis system. Dev. Comp. Immunol. 35:603–10 [Google Scholar]
  54. Earnshaw WC, Martins LM, Kaufmann SH. 54.  1999. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68:383–424 [Google Scholar]
  55. Muro I, Hay BA, Clem RJ. 55.  2002. The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC. J. Biol. Chem. 277:49644–50 [Google Scholar]
  56. Renault T, Faury N, Barbosa-Solomieu V, Moreau K. 56.  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. 35:725–35 [Google Scholar]
  57. Segarra A, Mauduit F, Faury N, Trancart S, Degremont L. 57.  et al. 2014. Dual transcriptomics of virus-host interactions: comparing two Pacific oyster families presenting contrasted susceptibility to ostreid herpesvirus 1. BMC Genomics 15:580 [Google Scholar]
  58. Xiang Z, Qu F, Wang F, Xiao S, Jun L. 58.  et al. 2015. ChBax/Bak as key regulators of the mitochondrial apoptotic pathway: cloned and characterized in Crassostrea hongkongensis. Fish Shellfish Immunol. 42:225–32 [Google Scholar]
  59. Moreno E, Yan M, Basler K. 59.  2002. Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr. Biol. 12:1263–68 [Google Scholar]
  60. Yuan S, Liu H, Gu M, Xu L, Huang S. 60.  et al. 2010. Characterization of the extrinsic apoptotic pathway in the basal chordate amphioxus. Sci. Signal. 3:ra66 [Google Scholar]
  61. Su J, Qiu L, Li L, Liu L, Wang L. 61.  et al. 2011. cDNA cloning and characterization of a new member of the tumor necrosis factor receptor family gene from scallop, Chlamys farreri. Mol. Biol. Rep. 38:4483–90 [Google Scholar]
  62. Zhang L, Li L, Guo X, Litman GW, Dishaw LJ, Zhang G. 62.  2015. Massive expansion and functional divergence of innate immune genes in a protostome. Sci. Rep. 5:8693 [Google Scholar]
  63. Xiang Z, Qu F, Qi L, Zhang Y, Tong Y, Yu Z. 63.  2013. Cloning, characterization and expression analysis of a caspase-8 like gene from the Hong Kong oyster, Crassostrea hongkongensis. Fish Shellfish Immun. 35:61797–803 [Google Scholar]
  64. Knowles G, Handlinger J, Jones B, Moltschaniwskyj N. 64.  2014. Hemolymph chemistry and histopathological changes in Pacific oysters (Crassostrea gigas) in response to low salinity stress. J. Invertebr. Pathol. 121:78–84 [Google Scholar]
  65. Shumway SE. 65.  1977. Effect of salinity fluctuation on osmotic-pressure and Na+, Ca2+ and Mg2+ ion concentrations in hemolymph of bivalve mollusks. Mar. Biol. 41:153–77 [Google Scholar]
  66. Jo PG, Choi CY. 66.  2008. Osmoregulation and mRNA expression of calcitonin-related receptor in the Pacific oyster Crassostrea gigas. Molluscan Res 28:137–41 [Google Scholar]
  67. Zhao X, Yu H, Kong L, Li Q. 67.  2012. Transcriptomic responses to salinity stress in the Pacific oyster Crassostrea gigas. PLOS ONE 7:e46244 [Google Scholar]
  68. Zhu JK. 68.  2001. Plant salt tolerance. Trends Plant Sci. 6:66–71 [Google Scholar]
  69. Berger VJ, Kharazova AD. 69.  1997. Mechanisms of salinity adaptations in marine molluscs. Hydrobiologia 355:115–26 [Google Scholar]
  70. Hosoi M, Kubota S, Toyohara M, Toyohara H, Hayashi I. 70.  2003. Effect of salinity change on free amino acid content in Pacific oyster. Fish. Sci. 69:395–400 [Google Scholar]
  71. Chen R, Yang F, Wang C. 71.  1999. Analysis of nutritions contents of oyster. J. Oceanogr. Taiwan Strait 18:195–98 [Google Scholar]
  72. Pierce SK, Rowlandfaux LM, Crombie BN. 72.  1995. The mechanism of glycine betaine regulation in response to hyperosmotic stress in oyster mitochondria—a comparative study of Atlantic and Chesapeake Bay oysters. J. Exp. Zool. 271:161–70 [Google Scholar]
  73. Boutet I, Meistertzheim AL, Tanguy A, Thebault MT, Moraga D. 73.  2005. Molecular characterization and expression of the gene encoding aspartate aminotransferase from the Pacific oyster Crassostrea gigas exposed to environmental stressors. Comp. Biochem. Phys. C 140:69–78 [Google Scholar]
  74. Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA. 74.  2012. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar. Environ. Res. 79:1–15 [Google Scholar]
  75. Tamayo D, Corporeau C, Petton B, Quere C, Pernet F. 75.  2014. Physiological changes in Pacific oyster Crassostrea gigas exposed to the herpesvirus OsHV-1μVar. Aquaculture 432:304–10 [Google Scholar]
  76. Ivanina AV, Froelich B, Williams T, Sokolov EP, Oliver JD, Sokolova IM. 76.  2011. Interactive effects of cadmium and hypoxia on metabolic responses and bacterial loads of eastern oysters Crassostrea virginica Gmelin. Chemosphere 82:377–89 [Google Scholar]
  77. Hochachka PW. 77.  1987. Metabolic Arrest and the Control of Biological Time Cambridge, MA: Harvard Univ. Press
  78. Nell JA, Cox E, Smith IR, Maguire GB. 78.  1994. Studies on triploid oysters in Australia. I. The farming potential of triploid Sydney rock oysters Saccostrea commercialis (Iredale and Roughley). Aquaculture 126:243–55 [Google Scholar]
  79. Akashige S. 79.  1992. Growth, survival, and glycogen content of triploid Pacific oyster Crassostrea gigas in the waters of Hiroshima, Japan. Nippon Suisan Gakk 58:1063–71 [Google Scholar]
  80. Corporeau C, Tamayo D, Pernet F, Quéré C, Madec S. 80.  2014. Proteomic signatures of the oyster metabolic response to herpesvirus OsHV-1 μVar infection. J. Proteomics 109:176–87 [Google Scholar]
  81. Le Moullac G, Queau I, Le Souchu P, Pouvreau S, Moal J. 81.  et al. 2007. Metabolic adjustments in the oyster Crassostrea gigas according to oxygen level and temperature. Mar. Biol. Res. 3:357–66 [Google Scholar]
  82. Tomanek L, Zuzow MJ, Ivanina AV, Beniash E, Sokolova IM. 82.  2011. Proteomic response to elevated PCO2 level in eastern oysters, Crassostrea virginica: evidence for oxidative stress. J. Exp. Biol. 214:1836–44 [Google Scholar]
  83. Chapman RW, Mancia A, Beal M, Veloso A, Rathburn C. 83.  et al. 2011. The transcriptomic responses of the eastern oyster, Crassostrea virginica, to environmental conditions. Mol. Ecol. 20:1431–49 [Google Scholar]
  84. Sussarellu R, Fabioux C, Le Moullac G, Fleury E, Moraga D. 84.  2010. Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar. Genom. 3:133–43 [Google Scholar]
  85. Chaney ML, Gracey AY. 85.  2011. Mass mortality in Pacific oysters is associated with a specific gene expression signature. Mol. Ecol. 20:2942–54 [Google Scholar]
  86. Tomanek L. 86.  2014. Proteomics to study adaptations in marine organisms to environmental stress. J. Proteomics 105:92–106 [Google Scholar]
  87. Kluytmans JH, Zandee DI. 87.  1983. Comparative study of the formation and excretion of anaerobic fermentation products in bivalves and gastropods. Comp. Biochem. Phys. B 75:729–32 [Google Scholar]
  88. Willmer P. 88.  2002. Biochemical adaptation—mechanism and process in physiological evolution. Science 296:473–75 [Google Scholar]
  89. Sussarellu R, Fabioux C, Camacho Sanchez M, Le Goïc N, Lambert C. 89.  et al. 2012. Molecular and cellular response to short-term oxygen variations in the Pacific oyster Crassostrea gigas. J. Exp. Mar. Biol. Ecol. 412:87–95 [Google Scholar]
  90. Guévélou E, Huvet A, Sussarellu R, Milan M, Guo X. 90.  et al. 2013. Regulation of a truncated isoform of AMP-activated protein kinase α (AMPKα) in response to hypoxia in the muscle of Pacific oyster Crassostrea gigas. J. Comp. Physiol. B 183:597–611 [Google Scholar]
  91. Dudognon T, Soudant P, Seguineau C, Quéré C, Auffret M, Kraffe E. 91.  2013. Functional capacities of gill mitochondria in oyster Crassostrea gigas during an emersion/immersion tidal cycle. Aquat. Living Resour. 26:249–56 [Google Scholar]
  92. Le Moullac G, Bacca H, Huvet A, Moal J, Pouvreau S, Van Wormhoudt A. 92.  2007. Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia. J. Exp. Zool. A 307A:371–82 [Google Scholar]
  93. Hardie DG, Scott JW, Pan DA, Hudson ER. 93.  2003. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 546:113–20 [Google Scholar]
  94. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N. 94.  et al. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15:6541–51 [Google Scholar]
  95. Majmundar AJ, Wong WJ, Simon MC. 95.  2010. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 40:294–309 [Google Scholar]
  96. Piontkivska H, Chung JS, Ivanina AV, Sokolov EP, Techa S, Sokolova IM. 96.  2011. Molecular characterization and mRNA expression of two key enzymes of hypoxia-sensing pathways in eastern oysters Crassostrea virginica (Gmelin): hypoxia-inducible factor α (HIF-α) and HIF-prolyl hydroxylase (PHD). Comp. Biochem. Phys. D 6:103–14 [Google Scholar]
  97. Kawabe S, Yokoyama Y. 97.  2012. Role of hypoxia-inducible factor α in response to hypoxia and heat shock in the Pacific oyster Crassostrea gigas. Mar. Biotechnol. 14:106–19 [Google Scholar]
  98. Meng J, Zhang LL, Huang BY, Li L, Zhang GF. 98.  2015. Comparative analysis of oyster (Crassostrea gigas) immune responses under challenge by different Vibrio strains and conditions. Molluscan Res. 35:1–11 [Google Scholar]
  99. Degremont L, Benabdelmouna A. 99.  2014. Mortality associated with OsHV-1 in spat Crassostrea gigas: role of wild-caught spat in the horizontal transmission of the disease. Aquacult. Int. 22:1767–81 [Google Scholar]
  100. Hoebe K, Janssen E, Beutler B. 100.  2004. The interface between innate and adaptive immunity. Nat. Immunol. 5:971–74 [Google Scholar]
  101. Takeuchi O, Akira S. 101.  2010. Pattern recognition receptors and inflammation. Cell 140:805–20 [Google Scholar]
  102. Kumar H, Kawai T, Akira S. 102.  2009. Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 388:621–25 [Google Scholar]
  103. Zhang Y, He X, Yu F, Xiang Z, Li J. 103.  et al. 2013. Characteristic and functional analysis of Toll-like receptors (TLRs) in the lophotrocozoan, Crassostrea gigas, reveals ancient origin of TLR-mediated innate immunity. PLOS ONE 8:e76464 [Google Scholar]
  104. Green TJ, Montagnani C, Benkendorff K, Robinson N, Speck P. 104.  2014. Ontogeny and water temperature influences the antiviral response of the Pacific oyster, Crassostrea gigas. Fish Shellfish Immunol. 36:151–57 [Google Scholar]
  105. Green TJ, Montagnani C. 105.  2013. Poly I:C induces a protective antiviral immune response in the Pacific oyster (Crassostrea gigas) against subsequent challenge with Ostreid herpesvirus (OsHV-1 μvar). Fish Shellfish Immunol. 35:382–88 [Google Scholar]
  106. Takeuchi O, Akira S. 106.  2009. Innate immunity to virus infection. Immunol. Rev. 227:75–86 [Google Scholar]
  107. Zemirli N, Arnoult D. 107.  2012. Mitochondrial anti-viral immunity. Int. J. Biochem. Cell Biol. 44:1473–76 [Google Scholar]
  108. Zhang Y, Yu F, Li J, Tong Y, Yu Z. 108.  2014. The first invertebrate RIG-I-like receptor (RLR) homolog gene in the pacific oyster Crassostrea gigas. Fish Shellfish Immunol. 40:466–71 [Google Scholar]
  109. Zhang Y, Yu Z. 109.  2013. The first evidence of positive selection in peptidoglycan recognition protein (PGRP) genes of Crassostrea gigas. Fish Shellfish Immunol. 34:1352–55 [Google Scholar]
  110. Itoh N, Takahashi KG. 110.  2008. Distribution of multiple peptidoglycan recognition proteins in the tissues of Pacific oyster, Crassostrea gigas. Comp. Biochem. Physiol. B 150:409–17 [Google Scholar]
  111. Itoh N, Takahashi KG. 111.  2009. A novel peptidoglycan recognition protein containing a goose-type lysozyme domain from the Pacific oyster, Crassostrea gigas. Mol. Immunol. 46:1768–74 [Google Scholar]
  112. Iizuka M, Nagasaki T, Takahashi KG, Osada M, Itoh N. 112.  2014. Involvement of Pacific oyster CgPGRP-S1S in bacterial recognition, agglutination and granulocyte degranulation. Dev. Comp. Immunol. 43:30–34 [Google Scholar]
  113. Jing X, Espinosa EP, Perrigault M, Allam B. 113.  2011. Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica. Fish Shellfish Immunol. 30:851–58 [Google Scholar]
  114. He X, Zhang Y, Yu F, Yu Z. 114.  2011. A novel sialic acid binding lectin with anti-bacterial activity from the Hong Kong oyster (Crassostrea hongkongensis). Fish Shellfish Immunol. 31:1247–50 [Google Scholar]
  115. Gueguen Y, Herpin A, Aumelas A, Garnier J, Fievet J. 115.  et al. 2006. Characterization of a defensin from the oyster Crassostrea gigas. Recombinant production, folding, solution structure, antimicrobial activities, and gene expression. J. Biol. Chem. 281:313–23 [Google Scholar]
  116. Gonzalez M, Gueguen Y, Desserre G, de Lorgeril J, Romestand B, Bachere E. 116.  2007. Molecular characterization of two isoforms of defensin from hemocytes of the oyster Crassostrea gigas. Dev. Comp. Immunol. 31:332–39 [Google Scholar]
  117. Gueguen Y, Bernard R, Julie F, Paulina S, Delphine DG. 117.  et al. 2009. Oyster hemocytes express a proline-rich peptide displaying synergistic antimicrobial activity with a defensin. Mol. Immunol. 46:516–22 [Google Scholar]
  118. Gonzalez M, Gueguen Y, Destoumieux-Garzon D, Romestand B, Fievet J. 118.  et al. 2007. Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI. PNAS 104:17759–64 [Google Scholar]
  119. Schmitt P, Gueguen Y, Desmarais E, Bachere E, de Lorgeril J. 119.  2010. Molecular diversity of antimicrobial effectors in the oyster Crassostrea gigas. BMC Evol. Biol. 10:23 [Google Scholar]
  120. Gerdol M, Venier P, Pallavicini A. 120.  2014. The genome of the Pacific oyster Crassostrea gigas brings new insights on the massive expansion of the C1q gene family in Bivalvia. Dev. Comp. Immunol. 49:59–71 [Google Scholar]
  121. Wang JF, Qi HG, Li L, Que HY, Wang D, Zhang GF. 121.  2015. Discovery and validation of genic single nucleotide polymorphisms in the Pacific oyster Crassostrea gigas. Mol. Ecol. Resour. 15:123–35 [Google Scholar]
  122. Zhang L, Li L, Zhang G. 122.  2012. Sequence variability of fibrinogen-related proteins (FREPs) in Crassostrea gigas. Chin. Sci. Bull. 57:3312–19 [Google Scholar]
  123. Huang B, Zhang L, Li L, Tang X, Zhang G. 123.  2015. Highly diverse fibrinogen-related proteins in the Pacific oyster Crassostrea gigas. Fish Shellfish Immunol. 43:485–90 [Google Scholar]
  124. Meng J, Zhu Q, Zhang L, Li C, Li L. 124.  et al. 2013. Genome and transcriptome analyses provide insight into the euryhaline adaptation mechanism of Crassostrea gigas. PLOS ONE 8:e58563 [Google Scholar]
  125. He Y, Yu H, Bao Z, Zhang Q, Guo X. 125.  2012. Mutation in promoter region of a serine protease inhibitor confers Perkinsus marinus resistance in the eastern oyster (Crassostrea virginica). Fish Shellfish Immunol. 33:411–17 [Google Scholar]
  126. Burdon D, Callaway R, Elliott M, Smith T, Wither A. 126.  2014. Mass mortalities in bivalve populations: a review of the edible cockle Cerastoderma edule (L.). Estuar. Coast. Shelf Sci. 150:271–80 [Google Scholar]
  127. Degremont L, Ernande B, Bedier E, Boudry P. 127.  2007. Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). I. Estimation of genetic parameters for survival and growth. Aquaculture 262:41–53 [Google Scholar]
  128. Zhang G, Li X, Xue Z. 128.  1999. The reasons of mass mortality of cultured shellfishes and its control approach in China. China Fish. 9:34–39 [Google Scholar]
  129. Xilin S, Jingwei S, Fugui W, Jun W, Jian W. 129.  et al. 2002. Reasons of mass death-off in Pacific oyster cultured in Dalian sea shore. J. Dalian Fish. Coll. 17:272–78 [Google Scholar]
  130. Friedman CS, Estes RM, Stokes NA, Burge CA, Hargove JS. 130.  et al. 2005. Herpes virus in juvenile Pacific oysters Crassostrea gigas from Tomales Bay, California, coincides with summer mortality episodes. Dis. Aquat. Organ. 63:33–41 [Google Scholar]
  131. Burge CA, Judah LR, Conquest LL, Griffin FJ, Cheney DP. 131.  et al. 2007. Summer seed mortality of the Pacific oyster, Crassostrea gigas Thunberg grown in Tomales Bay, California, USA: the influence of oyster stock, planting time, pathogens, and environmental stressors. J. Shellfish Res. 26:163–72 [Google Scholar]
  132. Schikorski D, Renault T, Saulnier D, Faury N, Moreau P, Pépin JF. 132.  2011. Experimental infection of Pacific oyster Crassostrea gigas spat by ostreid herpesvirus 1: demonstration of oyster spat susceptibility. Vet. Res. 42:1–13 [Google Scholar]
  133. Cheney DP, MacDonald BF, Elston RA. 133.  2000. Summer mortality of Pacific oysters, Crassostrea gigas (Thunberg): initial findings on multiple environmental stressors in Puget Sound, Washington, 1998. J. Shellfish Res. 19:353–59 [Google Scholar]
  134. Crisci C, Bensoussan N, Romano JC, Garrabou J. 134.  2011. Temperature anomalies and mortality events in marine communities: insights on factors behind differential mortality impacts in the NW Mediterranean. PLOS ONE 6:e23814 [Google Scholar]
  135. Berthelin C, Kellner K, Mathieu M. 135.  2000. Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (West Coast of France). Comp. Biochem. Phys. B 125:359–69 [Google Scholar]
  136. Mao YZ, Zhou Y, Yang HS, Wang RC. 136.  2006. Seasonal variation in metabolism of cultured Pacific oyster, Crassostrea gigas, in Sanggou Bay, China. Aquaculture 253:322–33 [Google Scholar]
  137. Li Y, Qin JG, Abbott CA, Li X, Benkendorff K. 137.  2007. Synergistic impacts of heat shock and spawning on the physiology and immune health of Crassostrea gigas: an explanation for summer mortality in Pacific oysters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293:R2353–62 [Google Scholar]
  138. Degremont L, Bedier E, Boudry P. 138.  2010. Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). II. Response to selection for survival and its influence on growth and yield. Aquaculture 299:21–29 [Google Scholar]
  139. Sanford E, Kelly MW. 139.  2011. Local adaptation in marine invertebrates. Annu. Rev. Mar. Sci. 3:509–35 [Google Scholar]
  140. Barranger A, Akcha F, Rouxel J, Brizard R, Maurouard E. 140.  et al. 2014. Study of genetic damage in the Japanese oyster induced by an environmentally-relevant exposure to diuron: evidence of vertical transmission of DNA damage. Aquat. Toxicol. 146:93–104 [Google Scholar]
  141. Weng NY, Wang WX. 141.  2014. Improved tolerance of metals in contaminated oyster larvae. Aquat. Toxicol. 146:61–69 [Google Scholar]
  142. Sanford E, Kelly MW. 142.  2011. Local adaptation in marine invertebrates. Annu. Rev. Mar. Sci. 3:509–35 [Google Scholar]
  143. Lord J, Whitlatch R. 143.  2014. Latitudinal patterns of shell thickness and metabolism in the eastern oyster Crassostrea virginica along the east coast of North America. Mar. Biol. 161:1487–97 [Google Scholar]
  144. Burford MO, Scarpa J, Cook BJ, Hare MP. 144.  2014. Local adaptation of a marine invertebrate with a high dispersal potential: evidence from a reciprocal transplant experiment of the eastern oyster Crassostrea virginica. Mar. Ecol. Progr. Ser. 505:161–75 [Google Scholar]
  145. Eierman L, Hare M. 145.  2013. Survival of oyster larvae in different salinities depends on source population within an estuary. J. Exp. Mar. Biol. Ecol. 449:61–68 [Google Scholar]
  146. Carnegie R, Reece KS. 146.  2012. Oyster population connectivity in lower Chesapeake Bay: possible impacts of disease selection in structuring populations. J. Shellfish Res. 31:267 [Google Scholar]
  147. Li L, Wu XY, Yu ZN. 147.  2013. Genetic diversity and substantial population differentiation in Crassostrea hongkongensis revealed by mitochondrial DNA. Mar. Genom. 11:31–37 [Google Scholar]
  148. Kim W-J, Dammannagoda ST, Jung H, Baek IS, Yoon HS, Choi SD. 148.  2014. Mitochondrial DNA sequence analysis from multiple gene fragments reveals genetic heterogeneity of Crassostrea ariakensis in East Asia. Genes Genomics 36:611–24 [Google Scholar]
  149. Rohfritsch A, Bierne N, Boudry P, Heurtebise S, Cornette F, Lapegue S. 149.  2013. Population genomics shed light on the demographic and adaptive histories of European invasion in the Pacific oyster, Crassostrea gigas. Evol. Appl. 6:1064–78 [Google Scholar]
  150. Ren J, Liu X, Jiang F, Guo X, Liu B. 150.  2010. Unusual conservation of mitochondrial gene order in Crassostrea oysters: evidence for recent speciation in Asia. BMC Evol. Biol. 10:394 [Google Scholar]
  151. Wang H, Qian L, Liu X, Zhang G, Guo X. 151.  2010. Classification of a common cupped oyster from Southern China. J. Shellfish Res. 29:857–66 [Google Scholar]
  152. Wang HY, Guo XM, Zhang GF, Zhang FS. 152.  2004. Classification of jinjiang oysters Crassostrea rivularis (Gould, 1861) from China, based on morphology and phylogenetic analysis. Aquaculture 242:137–55 [Google Scholar]
  153. Perry KJ, Henry JQ. 153.  2015. CRISPR/Cas9-mediated genome modification in the mollusc, Crepidula fornicata. Genesis 53:237–44 [Google Scholar]
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