Skip to main content
Log in

hsp90 and hsp47 appear to play an important role in minnow Puntius sophore for surviving in the hot spring run-off aquatic ecosystem

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Changes in the expression of a number of hsp genes in minnow Puntius sophore collected from a hot spring run-off (Atri hot spring in Odisha, India; 20o09′N 85°18′E, 36–38 °C) were investigated to study the upper thermal acclimation response under heat stress, using same species from aquaculture ponds (water temperature 27 °C) as control. Expression of hsp genes was analyzed in both groups using RT-qPCR, which showed up-regulation of hsp90 (2.1-fold) and hsp47 (2.5-fold) in hot spring run-off fishes, whereas there was no alteration in expression of other hsps. As the fish inhabit the hot spring run-off area for very long duration, they could have adapted to the environment. To test this hypothesis, fishes collected from hot spring run-off were divided into two groups; one was heat-shocked at 41 °C/24 h, and the other was acclimatized at 27 °C/24 h. Up-regulation of all the hsps (except hsp78) was observed in the heat-shocked fishes, whereas expression of all hsps was found to be down-regulated to the basal level in fishes maintained at 27 °C/24 h. Pathway analysis showed that the expressions of all the hsps except hsp90 are regulated by the transcription factor heat shock factor 1 (Hsf1). This study showed that hsp90 and hsp47 play an important role in Puntius sophore for surviving in the high-temperature environment of the hot spring run-off. Additionally, we show that plasticity in hsp gene expression is not lost in the hot spring run-off population.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    Article  CAS  PubMed  Google Scholar 

  • Arrigo A (2007) The cellular “networking” of mammalian HSP27 and its functions in the control of protein folding, redox state and apoptosis. Adv Exp Med Biol 594:14–26

    Article  PubMed  Google Scholar 

  • Barnes JA, Dix DJ, Collins BW, Luft C, Allen JW (2001) Expression of inducible Hsp70 enhances the proliferation of MCF-7 breast cancer cells and protects against the cytotoxic effects of hyperthermia. Cell Stress Chaperone 6(4):316–325

    Article  CAS  Google Scholar 

  • Basu N, Nakano T, Grau EG, Iwama GK (2001) The effects of cortisol on heat shock protein 70 levels in two fish species. Gen Comp Endocrinol 124:97–105

    Article  CAS  PubMed  Google Scholar 

  • Bonham RT, Fine MR, Pollock FM, Shelden EA (2003) HSP27, HSP70, and metallothionein in MDCK and LLC-PK1 renal epithelial cells: effects of prolonged exposure to cadmium. Toxicol Appl Pharmacol 191(1):63–73

    Article  CAS  PubMed  Google Scholar 

  • Boyd CE (1998) Water quality for pond aquaculture. International Center for Aquaculture and Aquatic Environment, Auburn University, Auburn, Albania http://www.extension.org/mediawiki/files/6/61/Water_Quality_for_Pond_Aquaculture.pdf

  • Brown SA, Kingston RE (1997) Disruption of downstream chromatin directed by a transcriptional activator. Genes Dev 11:3116–3121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley BA, Hofmann GE (2002) Thermal acclimation changes DNA-binding activity of heat shock factor 1(HSF1) in the goby Gillichthys mirabilis: implications for plasticity in the heat shock response in natural populations. J Exp Biol 205:3231–3240

    CAS  PubMed  Google Scholar 

  • Colson-Proch C, Morales A, Hervant F, Konecny L, Moulin C, Douady CJ (2010) First cellular approach of the effects of global warming on groundwater organisms: a study of the HSP70 gene expression. Cell Stress Chaperones 15(3):259–270

    Article  CAS  PubMed  Google Scholar 

  • CPCB (2007) Guidelines for water quality monitoring. Central Pollution Control Board, New Delhi

    Google Scholar 

  • Cuesta R, Laroia G, Schneider RJ (2000) Chaperone HSP27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev 14(12):1460–1470

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dahanukar N (2010) Puntius sophore. The IUCN Red List of Threatened Species 2010: e.T166623A6249514. http://dx.doi.org/10.2305/IUCN.UK.2010-4.RLTS.T166623A6249514.en

  • Dale Becker C, Genoway RG (1979) Evaluation of the critical thermal maximum for determining thermal tolerance of freshwater fish. Environ Biol Fish 4(3):245–256

    Article  Google Scholar 

  • Das T, Pal AK, Chakraborty SK, Manusha SM, Mukherjee SC (2005) Thermal tolerance and oxygen consumption of Indian major carps acclimated to four temperatures. J Therm Biol 29(3):157–163

    Article  Google Scholar 

  • Das A, Panda SS, Palita SK, Patra HK, Dhal NK (2012) Spatial and temporal variation of phytoplanktons in hot spring of Atri, Odisha, India. Curr Bot 3(5):35–40

    Google Scholar 

  • DeBolt S (2010) Copy number variation shapes genome diversity in Arabidopsis over immediate family generational scales. Genome Biol Evol 2:441–453

    Article  PubMed  PubMed Central  Google Scholar 

  • Denlinger DL, Rinehart JP, Yocum GD (2001) Stress proteins: a role in insect diapause? In: Denlinger DL, Giebultowicz J, Saunders DS (eds) Insect timing: circadian rhythmicity to seasonality. Elsevier, Amsterdam, pp 155–171

    Chapter  Google Scholar 

  • Dong Y, Dong S, Ji T (2008) Effect of different thermal regimes on growth and physiological performance of the sea cucumber Apostichopus japonicus Selenka. Aquaculture 275(1–4):329–334

    Article  Google Scholar 

  • Elliot JM, Elliot JA (1995) The effect of the rate of temperature increase on the critical thermal maximum for parr of Atlantic salmon and brown trout. J Fish Biol. doi:10.1111/j.1095-8649.1995.tb06014.x

    Google Scholar 

  • Fangue NA, Hofmeister M, Schulte PM (2006) Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859–2872

    Article  CAS  PubMed  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Ann Rev Physiol 61:243–282

    Article  CAS  Google Scholar 

  • Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79(2):425–449

    CAS  PubMed  Google Scholar 

  • Haslbeck M, Vierling E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Bio 427(7):1537–1548

    Article  CAS  Google Scholar 

  • http://www.pathwaycommons.org/about/. Accessed 15 Jan 2016

  • Iwama GK, Vijayan MM, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. Am Zool 39:901–909

    Article  CAS  Google Scholar 

  • Iwama GK, Afonso LOB, Todgham A, Ackerman P, Kazumi Nakano K (2004) Are hsps suitable for indicating stressed states in fish? J Exp Biol 207:15–19

    Article  CAS  PubMed  Google Scholar 

  • James TC, Usher J, Campbell S, Bond U (2008) Lager yeasts possess dynamic genomes that undergo rearrangements and gene amplification in response to stress. Curr Genet 53:139–152

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi K, Yamashita M, Watabe S, Aida K (1995) The warm temperature acclimation-related 65-kDa protein, Wap65, in goldfish and its gene expression. J Biol Chem 270(29):17087–17092

    Article  CAS  PubMed  Google Scholar 

  • Kondrashov FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc R Soc B. doi:10.1098/rspb.2012.1108

    Google Scholar 

  • Kregel KCJ (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92(5):2177–2186

    Article  CAS  PubMed  Google Scholar 

  • Kubista M, Andrade JM, Bengtsson M, Forootan A, Jonak J, Lind K et al (2006) The real-time polymerase chain reaction. Mol Asp Med 27:95e125

    Article  Google Scholar 

  • Leach MD, Budge S, Walker L, Munro C, Cowen LE, Brown AJP (2012) Hsp90 orchestrates transcriptional regulation by Hsf1 and cell wall remodelling by MAPK signalling during thermal adaptation in a pathogenic yeast. PLoS ONE 8(12):e1003069

    CAS  Google Scholar 

  • Li J, Soroka J, Buchner J (2012) The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim Biophys Acta 1823(3):624–635

    Article  CAS  PubMed  Google Scholar 

  • Lindquist S, Craig E (1988) The heat-shock proteins. Annu Rev Genet 22:631–677

    Article  CAS  PubMed  Google Scholar 

  • Logan CA, Buckley BA (2015) Transcriptomic responses to environmental temperature in eurythermal and stenothermal fishes. J Exp Biol 218:1915–1924

    Article  PubMed  Google Scholar 

  • Mahanty A, Ganguly S, Verma A, Sahoo S, Paria P, Mitra P, Singh BK, Sharma AP, Mohanty BP (2014) Nutrient profile of small indigenous fish Puntius sophore: proximate composition, amino acid, fatty acid and micronutrient profiles. Natl Acad Sci Lett 37(1):39–44

    Article  CAS  Google Scholar 

  • Mailhos C, Howard MK, Latchman DS (1994) Heat shock proteins hsp90 and hsp70 protect neuronal cells from thermal stress but not from programmed cell death. J Neurochem 63(5):1787–1795

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Paz P, Morales M, Martín R, Martínez-Guitarte JL, Morcillo G (2014) Characterization of the small heat shock protein Hsp27 gene in Chironomus riparius (Diptera) and its expression profile in response to temperature changes and xenobiotic exposures. Cell Stress Chaperones 19:529–540

    Article  PubMed  Google Scholar 

  • McDiarmid RW, Altig R (1999) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, p 202

    Google Scholar 

  • Meffe GK, Weeks SC, Mulvey M, Kandl KL (1995) Genetic differences in thermal tolerance of eastern mosqyitofish (Gambusia holbrooki; Poeciliidae) from ambient and thermal ponds. Can J Fish Aquat Sci 52(12):2704–2727

    Article  Google Scholar 

  • Meyer A, Biermann CH, Orti G (1993) The phylogenetic position of the zebrafish (Danio rerio), a model system in developmental biology: an invitation to the comparative method. Proc Biol Sci 252(1335):231–236

    Article  CAS  PubMed  Google Scholar 

  • Mohanty S, Mahanty A, Yadav RP, Purohit GK, Mohanty BN, Mohanty BP (2014) The Atri hot spring in Odisha—a natural ecosystem for global warming research. Int J Geol Earth Environ Sci 4:85–90

    Google Scholar 

  • Mohanty BP, Mitra T, Banerjee S, Bhattacharjee S, Mahanty A, Ganguly S, Purohit GK, Karunakaran D, Mohanty S (2015) Proteomic profiling of white muscle from freshwater catfish Rita rita. Physiol Biochem 41:789–802

    CAS  Google Scholar 

  • Mounier N, Arrigo AP (2002) Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperone 7(2):167–176

    Article  CAS  Google Scholar 

  • Nakano K, Iwama GK (2002) The 70- kDa heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: relationship of hsp70 and thermal tolerance. Comp Biochem Physiol A 133:79–94

    Article  Google Scholar 

  • Norris CE, diLorio PJ, Schultz RJ, Hightower LE (1995) Variation in heat shock protein within tropical and desert species of Poeciliid fishes. Mol Biol Evol 12(6):1048–1062

    CAS  PubMed  Google Scholar 

  • Ojima N, Yamashita M, Watabe S (2005) Quantitative mRNA expression profiling of heat-shock protein families in rainbow trout cells. Biochem Biophys Res Commun 329(1):51–57

    Article  CAS  PubMed  Google Scholar 

  • Oksala NKJ, Ekmekçi FG, Ozsoy E, Kirankaya S, Kokkola T, Emecen G, Lappalainen J, Kaarniranta K, Atalay M (2014) Natural thermal adaptation increases heat shock protein levels and decreases oxidative stress. Redox Biol 3:25–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panda SK, Jyoti V, Bhadra B, Nayak KC, Shivaji S, Rainey FA, Das SK (2009) Thiomonas bhubaneswarensis sp. nov., an obligately mixotrophic, moderately thermophilic, thiosulfate-oxidizing bacterium. Int J Syst Evol Microbiol 59:2171–2175

    Article  CAS  PubMed  Google Scholar 

  • Pearl LH, Prodromou C (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75:271–294

    Article  CAS  PubMed  Google Scholar 

  • Pearson WDS, Kulyk M, Kelly GM, Krone PH (1996) Cloning and characterization of a cDNA encoding the collagen-binding stress protein HSP47 in zebrafish. DNA Cell Biol 15(3):263–272

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pirkkala L, Nykanen P, Sistonen L (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15:1118–1131

    Article  CAS  PubMed  Google Scholar 

  • Podrabsky JE, Somero GN (2004) 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

    Article  CAS  PubMed  Google Scholar 

  • Purohit GK, Mahanty A, Suar M, Sharma AP, Mohanty BP, Mohanty S (2014) Investigating hsp gene expression in liver of channa striatus under heat stress for understanding the upper thermal acclimation. Biomed Res Int 2014:381719. doi:10.1155/2014/381719

    Article  PubMed  PubMed Central  Google Scholar 

  • Purohit GK, Mahanty A, Mohanty BP, Mohanty S (2015) Evaluation of housekeeping genes as references for quantitative real-time PCR analysis of gene expression in the murrel Channa striatus under high-temperature stress. Fish Physiol Biochem. doi:10.1007/s10695-015-0123-0

    Google Scholar 

  • Reddy DV, Nagbhushanam P, Ramesh G (2013) Turnover time of Tural and Rajvadi hot spring waters, Maharashtra, India. Curr Sci 104(10):1419–1424

    CAS  Google Scholar 

  • Roberts R, Agius C, Saliba C, Bossier P, Sung Y (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33(10):789–801

    Article  CAS  PubMed  Google Scholar 

  • Sanders BM, Martin LS, Wakagawa PA, Hunter DA, Miller S, Ullrich SJ (1994) Specific cross-reactivity of antibodies raised against two major stress proteins, stress 70 and chaperonin 60, in diverse species. Environ Toxicol Chem 13(8):1241–1249

    Article  CAS  Google Scholar 

  • Schuster-Bockler B, Conrad D, Bateman A (2010) Dosage sensitivity shapes the evolution of copy-number varied regions. PLoS ONE 5:e9474

    Article  PubMed  PubMed Central  Google Scholar 

  • Shamovsky I, Nudler E (2008) New insights into the mechanism of heat shock response activation. Cell Mol Life Sci 65:855–861

    Article  CAS  PubMed  Google Scholar 

  • Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920

    Article  CAS  PubMed  Google Scholar 

  • Stone NM, Thomforde HK (2004) Understanding Your Fish Pond Water Analysis Report. Cooperative Extension Program, University of Arkansas at Pine Bluff Aquaculture/Fisheries

  • Tedeschi JN, Kennington WJ, Berry O, Whiting S, Meekan M, Mitchell NJ (2015) Increased expression of Hsp70 and Hsp90 mRNA as biomarkers of thermal stress in loggerhead turtle embryos (Caretta Caretta). J Therm Biol 47:42–50

    Article  CAS  PubMed  Google Scholar 

  • Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971–979

    Article  CAS  PubMed  Google Scholar 

  • Tomanek L, Somero GN (2002) Interspecific- and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression. J Exp Biol 205(5):677–685

    CAS  PubMed  Google Scholar 

  • Tosab M, Batten MR, Bulleid NJ (2000) Hsp47: a molecular chaperone that interacts with and stabilizes correctly-folded procollagen. EMBO J 19(10):2204–2211

    Article  Google Scholar 

  • Vihervaara A, Sistonen L (2014) HSF1 at a glance. J Cell Sci 127:261–266

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Dai AY, Tao K, Xiao Q, Huang ZL, Gao M, Li H, Wang X, Cao WX, Feng WL (2015) Heat shock protein-70 neutralizes apoptosis inducing factor in Bcr/Abl expressing cells. Cell Signal 27(10):1949–1955

    Article  CAS  PubMed  Google Scholar 

  • Zeiner M, Cindric IJ, Pozgaj M, Pirkl R, Silic T, Stingeder G (2015) Influence of soil composition on the major, minor and trace metal content of Velebit biomedical plants. J Pharm Biomed Anal 106:153–158

    Article  CAS  PubMed  Google Scholar 

  • Zunino B, Rubio-Patiño C, Villa E, Meynet O, Proics E, Cornille A, Pommier S, Mondragón L, Chiche J, Bereder J-M, Carles M, Ricci J-E (2016) Hyperthermic intraperitoneal chemotherapy leads to an anticancer immune response via exposure of cell surface heat shock protein 90. Oncogene 35:261–268

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by the Indian Council of Agricultural Research under the National Fund for Basic, Strategic and Frontier Application Research in Agriculture (NFBSFARA; recently renamed National Agricultural Science Fund, NASF) Project # AS-2001 (B.P.M. and S.M). A.M. and G.K.P. are NFBSFARA Senior Research Fellows. The authors are thankful to Director, ICAR—Central Inland Fisheries Research Institute, Barrackpore, and Director, School of Biotechnology, KIIT University, Bhubaneswar, for the facilities and encouragement. Technical assistance received from Shri Laddu Ram Mahaver, Samir K. Paul and Rabiul Sk. is acknowledged. The authors would like to acknowledge the anonymous reviewers for critically reviewing the manuscript; the constructive criticism and suggestions from the reviewers have resulted in substantial improvement of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bimal Prasanna Mohanty.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 58 kb)

Supplementary material 2 (DOC 47 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mahanty, A., Purohit, G.K., Yadav, R.P. et al. hsp90 and hsp47 appear to play an important role in minnow Puntius sophore for surviving in the hot spring run-off aquatic ecosystem. Fish Physiol Biochem 43, 89–102 (2017). https://doi.org/10.1007/s10695-016-0270-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0270-y

Keywords

Navigation