Skip to main content
Log in

The Effect of Temperature Stress on Development and Heat-shock Protein Expression in Larval Green Sturgeon (Acipenser mirostris)

  • Green Sturgeon
  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Water temperature is an important environmental variable influencing the distribution and health of coldwater fishes such as the green sturgeon, Acipenser medirostris. In this study, we investigated if larval sturgeon were able to tolerate or recover from acute, non-lethal temperature stress that commonly causes deformed notochords, and sought to identify the role of heat-shock proteins (hsp) in stress tolerance. The hsp response is one of the most important cellular mechanisms to prevent the damaging effects of thermal cellular stress, and differences in the ability to over-express hsps during stressful conditions may be associated with an organism’s vulnerability and the extent of thermal injury. In this study, newly hatched larvae were maintained at 17°C (control), or exposed to (a) 26°C for 3 d then maintained at 17°C until yolk-sac absorption or (b) 26°C until yolk-sac absorption. Individuals with deformed notochords were counted, and hsp60, 72, 78 and 89 were analyzed in both normal and deformed larvae by western blotting. Approximately 33% of fish developed curved notochords within the first 3 d of exposure to 26°C. After transfer to cool water 16.5% showed deformities at stage 45, suggesting a significant number of larvae had recovered. Hsp levels remained elevated for at least 9 days after termination of heat-exposure. Overall, percentage of deformed larvae, and hsp72/hsp78 levels were highest in fish continuously exposed to 26°C until yolk-sac absorption. Deformed individuals had significantly higher expression levels of hsp72 and hsp78, and lower hsp60 levels than normal larvae. We conclude that expression of hsp72 and hsp78 and potentially hsp60 are linked to phenotypic variation in the response and vulnerability of green sturgeon larvae to thermal stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Artyukhin EN, Andronov AE (1990) A morphological study of the green sturgeon, Acipenser medirostris (Chondrostei, Acipenseridae), from the Tumnin (Datta) River and some aspects of the ecology and␣zoogeography of Acipenseridae. J Ichthyol 30:11–21

    Google Scholar 

  • Baltz DM, Vondracek B, Brown LR, Moyle PB (1987) Influence of temperature on microhabitat choice by fishes in a California stream. Trans Am Fisher Soc 116:12–20

    Article  Google Scholar 

  • Bartholow JM (2005) Recent water temperature trends in the Lower Klamath River, Ca. North Am J Fisher Manage 25:152–162

    Article  Google Scholar 

  • Birstein VJ (1993) Sturgeons and paddlefishes: threatened fishes in need of conservation. Conserv Biol 7:773–787

    Article  Google Scholar 

  • Blattler DP, Garner F, Van Slyke K, Bradley A (1972) Quantitative electrophoresis in polyacrylamide gels of 2–40%. J Chromatogr 64:147–155

    Article  CAS  Google Scholar 

  • Buckley BA, Hofmann GE (2004) Magnitude and duration of thermal stress determine kinetics of hsp gene regulation in the goby Gillichthys mirabilis. Physiol Biochem Zool 77(4):570–581

    Article  CAS  Google Scholar 

  • Campbell RR (1997) Rare and endangered fishes and marine mammals of Canada: COSEWIC Fish and Marine Mammal Subcommittee Status Reports: XI. Can Field-Natural 111:249–257

    Google Scholar 

  • Cleaver O, Seufert DW, Krieg PA (2000) Endoderm patterning by the notochord: development of the hypochord in Xenopus. Development 127:869–879

    CAS  Google Scholar 

  • Deng X, van Eenennaam JP, Doroshov SI (2002). Comparison of early life stages and growth of green and white sturgeon. In van Winkle W, Anders PJ, Secor DH, Dixon DA (eds) Biology, management and protection of North American Sturgeon. American Fisheries Society, Symposium 28, Bethesda, Maryland, pp 237–248

    CAS  Google Scholar 

  • Dettlaff TA, Ginsburg AS, Schmalhausen OI (1993) Sturgeon fishes: developmental biology and aquaculture. Springer-Verlag, New York

    Google Scholar 

  • Dietz TJ, Somero GN (1992) The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). Proc Natl Acad Sci USA 89:3389–3393

    Article  CAS  Google Scholar 

  • Feige U, Morimoto RI, Yahara I, Polla BS (eds) (1996) Stress-inducible cellular responses. Birkhauser Verlag, Basel, Switzerland

    Google Scholar 

  • Hallare AV, Pagulayan R, Lacdan N, Koehler H-R, Triebskorn R (2005) Assessing water quality in a tropical lake using biomarkers in zebrafish embryos: developmental toxicity and stress protein responses. Environ Monit Assess 104:171–187

    Article  Google Scholar 

  • Israel JA, Cordes JF, Blumberg MA, May B (2004) Geographic patterns of genetic differentiation among collections of green sturgeon. North Am J Fisher Manage 24:922–931

    Article  Google Scholar 

  • Iwama GK, Thomas PT, Forsyth RB, Vijayan MM (1998) Heat shock protein expression in fish. Rev Fish Biol Fish 8:35–56

    Article  Google Scholar 

  • Krone PH, Lele Z, Sass JB (1997) Heat shock genes and the heat shock response in zebrafish embryos. Biochem Cell Biol 75:487–497

    Article  Google Scholar 

  • Kynard B, Parker E, Parker T (2005) Behavior of early life intervals of Klamath River green sturgeon, Acipenser medirostris, with a note on body color. Environ Biol Fish 72:85–97

    Article  Google Scholar 

  • Laemmli UK (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  Google Scholar 

  • Lele Z, Engel S, Krone PH (1997) Hsp47 and hsp70 gene expression is differentially regulated in a stress- and tissue-specific manner in zebrafish embryos. Devel Genet 21:123–133

    Article  CAS  Google Scholar 

  • Long JH Jr (1995) Morphology, mechanics, and locomotion: the relation between the notochord and swimming motions in sturgeon. Environ Biol Fish 44:199–211

    Article  Google Scholar 

  • Long JH Jr, Koob-Edmunds M, Sinwell B, Koob TJ (2002) The notochord of hagfish Myxine glutinosa: visco-elastic properties and mechanical functions during steady swimming. J Exp Biol 205:3819–3831

    Google Scholar 

  • Martin CC, Tsang Ch, Beiko RG, Krone PH (2002) Expression and genomic organization of the zebrafish chaperonin gene complex. Genome 45:804–811

    Article  Google Scholar 

  • Mayfield RB, Cech JJ Jr (2004) Temperature effects on green sturgeon bioenergetics. Trans Am Fisher Soc 133:961–970

    Article  Google Scholar 

  • Morimoto RI, Tissieres A, Georgopoulos C (eds) (1990) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, USA

    Google Scholar 

  • Mookerjee S, Deuchar EM, Waddington CH (1953) The␣morphogenesis of the notochord in amphibia. J Embryol Exp Morphol 1(4):399–409

    Google Scholar 

  • Moyle PB (2002) Inland fishes of California. University of California Press, Berkeley, California

    Google Scholar 

  • NMFS (National Marine Fisheries Service) (2003). Endangered and threatened wildlife and plants: 12-month finding on a petition to list North American green sturgeon as threatened or endangered. Federal Register 68:(19):4433–4441

    Google Scholar 

  • NOAA (National Oceanic & Atmospheric Administration) (2005) Endangered and threatened wildlife and plants: proposed threatened status for southern distinct population segment of North American green sturgeon. Federal Register 70(65):17386–17401

    Google Scholar 

  • Nollen EAA, Morimoto RI (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci 115:2809–2816

    CAS  Google Scholar 

  • Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496

    Article  CAS  Google Scholar 

  • Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23: 49–75

    Article  CAS  Google Scholar 

  • Sarkar S, Lakhotia SC (2005) The Hsp60C gene in the 25 F cytogenitic region in Drosophila melanogaster is essential for tracheal development and fertility. J␣Genet 84(3):265–281

    CAS  Google Scholar 

  • Schmitz RJ (1998) Comparative ultrastructure of the cellular components of the unconstricted notochord in␣the sturgeon and the lungfish. J Morphol 236:75–104

    Article  Google Scholar 

  • Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits and costs of living. Integr Comp Biol 42:780–789

    Article  Google Scholar 

  • Van Eenennaam JP, Linares-Casenave J, Deng X, Doroshov SI (2005) Effect of incubation temperature on green sturgeon embryos, Acipenser medirostris. Environ Biol Fish 72:145–154

    Article  Google Scholar 

  • Van Eenennaam JP, Webb MAH, Deng X, Doroshov SI, Mayfield RB, Cech JJ Jr, Hillemeier DC, Willson TE (2001) Artificial spawning and larval rearing of Klamath River green sturgeon. Trans Am Fisher Soc 130:159–165

    Article  Google Scholar 

  • Viant MR, Werner I, Rosenblum ES, Gantner AS, Tjeerdema RS, Johnson ML (2003) Correlation between stress protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiol Biochem 29:159–171

    Article  CAS  Google Scholar 

  • Werner I, Koger CS, Hamm JT, Hinton DE (2001) Ontogeny of the heat shock protein, hsp70 and hsp60, response and developmental effects of heat shock in the teleost, medaka (Oryzias latipes). Environ Sci 8(1):13–29

    CAS  Google Scholar 

  • Werner I, Smith T, Feliciano J, Johnson ML (2005) Heat-shock proteins in juvenile steelhead trout (Oncorhynchus mykiss) reflect thermal conditions in the Navarro River watershed, California, USA. Trans Am Fisher Soc 134:399–410

    Article  CAS  Google Scholar 

  • Zuegel U, Kaufmann SHE (1999) Role of heat shock proteins in protection from and pathogenesis of infectious diseases. Clin Microbiol Rev 12(1):19–39

    Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the support of the Yurok Tribal Council and the Yurok Fisheries Program for supplying us with broodstock fish. Gina Lee provided valuable assistance in the laboratory, and we are grateful for Daniel Markiewicz for help with statistical analyses. Additional thanks to the Center for Aquatic Biology and Aquaculture for use of their research facilities. This project was funded by the CalFed Bay-Delta Program, contract # ERP-02D-P57.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Inge Werner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Werner, I., Linares-Casenave, J., Van Eenennaam, J.P. et al. The Effect of Temperature Stress on Development and Heat-shock Protein Expression in Larval Green Sturgeon (Acipenser mirostris). Environ Biol Fish 79, 191–200 (2007). https://doi.org/10.1007/s10641-006-9070-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-006-9070-z

Keywords

Navigation