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Transcriptome response of the Pacific oyster, Crassostrea gigas susceptible to thermal stress: A comparison with the response of tolerant oyster

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Abstract

Although oysters are exposed to seasonal temperature changes, they are frequently subjected to acute temperature stress during emersion due to their attachment on their rocky shore habitats. To understand the effect of acute temperature elevation on the whole transcriptome of susceptible Pacific oyster Crassostrea gigas over time, the oysters were exposed to temperatures ranging from the control 20°C to 32°C for 72 h. We compared the genome-wide patterns of mRNA expression of susceptible oysters with those obtained from thermotolerant oysters. RNA-seq identified differentially expressed stress responsive Gene Ontology (GO) terms and relevant transcripts following acute thermal stress. The clearest pattern between susceptible and tolerant oysters was the dramatic differences in transcriptional expression in the hsp70 gene family. GO terms and genes typically associated with oxygen binding were also repressed compared to those of tolerant oysters. This study provides insights into the significant differences in molecular response of susceptible C. gigas to acute heat stress, and the will further our understanding of the basis of molecular adaptation in the Pacific oyster.

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References

  1. Scholander, P. F., Flagg, W., Walters, V. & Irving, L. Climatic Adaptation in Arctic and Tropical Poikilotherms. Physiol Zool 26:67–92 (1953).

    Article  Google Scholar 

  2. Pörtner, H. O., Peck, L. & Somero, G. Thermal limits and adaptation in marine Antarctic ectotherms: an integrative view. Philos Trans R Soc Lond B Biol Sci 362:2233 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Shatkin, G., Shumway, S. & Hawes, R. Considerations regarding the possible introduction of the pacific oyster (Crassostrea gigas) to the Gulf of Maine: A review of global experience. Oceanograph Lit Rev 9:1677 (1998).

    Google Scholar 

  4. Ruesink, J. L. et al. Changes in productivity associated with four introduced species: ecosystem transformation of a ‘pristine’ estuary. Mar Ecol Prog Ser 311:203–215 (2006).

    Article  Google Scholar 

  5. Meistertzheim, A.-L., Tanguy, A., Moraga, D. & Thébault, M.-T. Identification of differentially expressed genes of the Pacific oyster Crassostrea gigas exposed to prolonged thermal stress. FEBS J 274:6392–6402 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Park, H., Ahn, I.-Y. & Lee, H. E. Expression of heat shock protein 70 in the thermally stressed Antarctic clam Laternula elliptica. Cell Stress Chaperones 12:275–282 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Clark, M. S., Fraser, K. P. P. & Peck, L. S. Antarctic marine molluscs do have an HSP70 heat shock response. Cell Stress Chaperones 13:39–49 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kim, M., Ahn, I.-Y., Kim, H., Cheon, J. & Park, H. Molecular characterization and induction of heat shock protein 90 in the Antarctic bivalve Laternula elliptica. Cell Stress Chaperones 14:363–370 (2009).

    Article  CAS  PubMed  Google Scholar 

  9. Farcy, É., Voiseux, C., Lebel, J.-M. & Fiévet, B. Transcriptional expression levels of cell stress marker genes in the Pacific oyster Crassostrea gigas exposed to acute thermal stress. Cell Stress Chaperones 14:371–380 (2009).

    Article  CAS  PubMed  Google Scholar 

  10. Truebano, M. et al. Transcriptional response to heat stress in the Antarctic bivalve Laternula elliptica. J Exp Mar Biol Ecol 391:65–72 (2010).

    Article  CAS  Google Scholar 

  11. Liu, D. & Chen, Z. The expression and induction of heat shock proteins in molluscs. Protein Pept Lett 20:602–606 (2013).

    Article  PubMed  Google Scholar 

  12. Chu, N. D., Miller, L. P., Kaluziak, S. T., Trussell, G. C. & Vollmer, S. V. Thermal stress and predation risk trigger distinct transcriptomic responses in the intertidal snail Nucella lapillus. Mol Ecol 23:6104–6113 (2014).

    Article  CAS  PubMed  Google Scholar 

  13. Gleason, L. U. & Burton, R. S. RNA-seq reveals regional differences in transcriptome response to heat stress in the marine snail Chlorostoma funebralis. Mol Ecol 24:610–627 (2015).

    Article  CAS  PubMed  Google Scholar 

  14. Zhu, Q., Zhang, L., Li, L., Que, H. & Zhang, G. Expression characterization of stress genes under high and low temperature stresses in the Pacific oyster, Crassostrea gigas. Mar Biotechnol 18:176–188 (2016).

    Article  CAS  PubMed  Google Scholar 

  15. Guo, X., He, Y., Zhang, L., Lelong, C. & Jouaux, A. Immune and stress responses in oysters with insights on adaptation. Fish Shellfish Immunol 46:107–119 (2015).

    Article  CAS  PubMed  Google Scholar 

  16. Mann, R., Burreson, E. M. & Baker, P. K. The decline of the virginia oyster fishery in chesapeake bay: Considerations for introduction of a non-endemic species, Crassostrea gigas (Thunberg, 1793). J Shellfish Res 10:379–388 (1991).

    Google Scholar 

  17. FAO, 2012. Cultured Aquatic Species Information Programme. Crassostrea gigas. Helm, M.M., In: FAO Fisheries and Aquaculture Department. Rome.

    Google Scholar 

  18. Shamseldin, A., Clegg, J. S., Friedman, C. S., Cherr, G. N. & Pillai, M. Induced thermotolerance in the Pacific oyster, Crassostrea gigas. J Shellfish Res 16:487–491 (1997).

    Google Scholar 

  19. Hamdoun, A. M., Cheney, D. P. & Cherr, G. N. 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 205:160–169 (2003).

    Article  CAS  PubMed  Google Scholar 

  20. Zhang, G. et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54 (2012).

    Article  CAS  PubMed  Google Scholar 

  21. Zhang, G. et al. Molecular basis for adaptation of oysters to stressful marine intertidal environments. Annu Rev Anim Biosci 4:357–381 (2016).

    Article  PubMed  Google Scholar 

  22. Clegg, J. et al. Induced thermotolerance and the heat shock protein-70 family in the Pacific oyster Crassostrea gigas. Mol Mar Biol Biotechnol 7:21–30 (1998).

    CAS  Google Scholar 

  23. Ivanina, A. V., Taylor, C. & Sokolova, I. M. Effects of elevated temperature and cadmium exposure on stress protein response in eastern oysters Crassostrea virginica (Gmelin). Aquat Toxicol 91:245–254 (2009).

    Article  CAS  PubMed  Google Scholar 

  24. Lang, R. P. et al. Transcriptome profiling of selectively bred Pacific oyster Crassostrea gigas families that differ in tolerance of heat shock. Mar Biotechnol 11:650–668 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Zhang, Y. et al. Proteomic basis of stress responses in the gills of the pacific oyster Crassostrea gigas. J Proteome Res 14:304–317 (2015).

    Article  CAS  PubMed  Google Scholar 

  26. Lim, H.-J. et al. Thermal stress induces a distinct transcriptome profile in the Pacific oyster Crassostrea gigas. Comp Biochem Physiol Part D 19:62–70 (2016).

    CAS  Google Scholar 

  27. Feder, M. E. & Hofmann, G. E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282 (1999).

    Article  CAS  PubMed  Google Scholar 

  28. Weber, R. E. & Vinogradov, S. N. Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81:569–628 (2001).

    CAS  PubMed  Google Scholar 

  29. Terwilliger, R. C., Terwilliger, N. B. & Arp, A. Thermal vent clam (Calyptogena magnifica) hemoglobin. Science 219:981–983 (1983).

    Article  CAS  PubMed  Google Scholar 

  30. Gavira, J. A. et al. Structure and ligand selection of hemoglobin II from Lucina pectinata. J Biol Chem 283:9414–9423 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bao, Y., Wang, Q. & Lin, Z. Hemoglobin of the bloody clam Tegillarca granosa (Tg-HbI) is involved in the immune response against bacterial infection. Fish Shellfish Immunol 31:517–523 (2011).

    Article  CAS  PubMed  Google Scholar 

  32. Ramos-Alvarez, C. et al. Reactivity and dynamics of H2S, NO, and O2 interacting with hemoglobins from Lucina pectinata. Biochemistry 52:7007–7021 (2013).

    Article  CAS  PubMed  Google Scholar 

  33. Xu, B. et al. Role of hemoglobin from blood clam Scapharca kagoshimensis beyond oxygen transport. Fish Shellfish Immunol 44:248–256 (2015).

    Article  CAS  PubMed  Google Scholar 

  34. Montes-Rodríguez, I. M., Rivera, L. E., López-Garriga, J. & Cadilla, C. L. Characterization and expression of the Lucina pectinata oxygen and sulfide Binding hemoglobin genes. PLoS ONE 11:e0147977 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Podrabsky, J. E. & Somero, G. N. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J Exp Biol 207:2237–2254 (2004).

    Article  CAS  PubMed  Google Scholar 

  36. Yao, C. L. & Somero, G. N. The impact of acute temperature stress on hemocytes of invasive and native mussels (Mytilus galloprovincialis and Mytilus californianus): DNA damage, membrane integrity, apoptosis and signaling pathways. J Exp Biol 215:4267–4277 (2012).

    Article  CAS  PubMed  Google Scholar 

  37. Park, M. S. et al. Effects of antifouling biocides on molecular and biochemical defense system in the gill of the pacific oyster Crassostrea gigas. PLoS ONE 11:e0168978 (2017).

    Article  Google Scholar 

  38. Lim, H.-J. et al. Transcriptome profiling of the Pacific oyster Crassostrea gigas by Illumina RNA-seq. Genes Genomics 38:359–365 (2015).

    Article  Google Scholar 

  39. Du, Y. et al. Validation of housekeeping genes as internal controls for studying gene expression during Pacific oyster (Crassostrea gigas) development by quantitative real-time PCR. Fish Shellfish Immunol 34:939–945 (2013).

    Article  CAS  PubMed  Google Scholar 

  40. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Unit of Polar Genomics, Korea Polar Research Institute, Incheon, 21990, Republic of Korea

    Bo-Mi Kim

  2. Division of Bioengineering, College of Life Sciences and Bioengineering, Incheon National University, Incheon, 22012, Republic of Korea

    Kyobum Kim

  3. Department of Agriculture and Life Industry, Kangwon National University, Chuncheon, 24341, Republic of Korea

    Ik-Young Choi

  4. Department of Marine Science, College of Natural Sciences, Incheon National University, Incheon, 22012, Republic of Korea

    Jae-Sung Rhee

  5. Research Institute of Basic Sciences, Incheon National University, Incheon, 22012, Republic of Korea

    Jae-Sung Rhee

  6. Institute of Green Environmental Research Center, 169, Gaetbeol-ro, Yeonsugu, Incheon, 21999, Republic of Korea

    Jae-Sung Rhee

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  1. Bo-Mi Kim
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  2. Kyobum Kim
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  4. Jae-Sung Rhee
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Correspondence to Ik-Young Choi or Jae-Sung Rhee.

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Kim, BM., Kim, K., Choi, IY. et al. Transcriptome response of the Pacific oyster, Crassostrea gigas susceptible to thermal stress: A comparison with the response of tolerant oyster. Mol. Cell. Toxicol. 13, 105–113 (2017). https://doi.org/10.1007/s13273-017-0011-z

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  • DOI: https://doi.org/10.1007/s13273-017-0011-z

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