Abstract
Land snails are subject to daily and seasonal variations in temperature and in water availability, and use heat shock proteins (HSPs) as part of their survival strategy. We used experimental heat stress to test whether adaptation to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desert species, Sphincterochila zonata, and a Mediterranean-type species, Sphincterochila cariosa. Our findings show that in S. cariosa, heat stress caused rapid induction of Hsp70 proteins and Hsp90 in the foot and kidney tissues, whereas the desert-inhabiting species S. zonata displayed delayed induction of Hsp70 proteins in the foot and upregulation of Hsp90 alone in the kidney. Our study suggests that Sphincterochila species use HSPs as part of their survival strategy following heat stress and that adaptation to different habitats results in the development of distinct strategies of HSP expression in response to heat, namely the reduced induction of HSPs in the desert-dwelling species. We suggest that the desert species S. zonata relies on mechanisms and adaptations other than HSP induction, thus avoiding the fitness consequences of continuous HSP upregulation.
References
Adhikari AS, Sridhar Rao K, Rangaraj N, Parnaik VK, Mohan Rao C (2004) Heat stress-induced localization of small heat shock proteins in mouse myoblasts: intranuclear lamin A/C speckles as target for alphaB-crystallin and Hsp25. Exp Cell Res 299 (2):393–403
Alastalo TP, Hellesuo M, Sandqvist A, Hietakangas V, Kallio M, Sistonen L (2003) Formation of nuclear stress granules involves HSF2 and coincides with the nucleolar localization of Hsp70. J Cell Sci 116 (Pt 17):3557–3570
Arad Z, Goldenberg S, Heller J (1989) Resistance to desiccation and distribution patterns in the land snail Sphincterochila. J Zool, London 218:353–364
Arad Z, Goldenberg S, Heller J (1992) Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the land snail Xeropicta vestalis J Zool, London 226:643–656
Arad Z, Goldenberg S, Avivi TR, Heller J (1993a) Intraspecific variation in resistance to desiccation in the land snail Theba pisana. Int J Biometeorol 37:183–189
Arad Z, Goldenberg S, Heller J (1993b) Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the bush-dwelling land snail Trochoidea simulata. J Zool, London 229:249–265
Arad Z, Mizrahi T, Goldenberg S, Heller J (2010) Natural annual cycle of heat shock proteins expression in land snails: desert vs. Mediterranean species of Sphincterochila. J Exp Biol 213:3487–3495
Beck FX, Neuhofer W, Muller E (2000) Molecular chaperones in the kidney: distribution, putative roles, and regulation. Amer J Physiol 279 (2):F203-215
Borkan SC, Gullans SR (2002) Molecular chaperones in the kidney. Ann Rev Physiol 64:503–527
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brooks SP, Storey KB (1995) Evidence for aestivation specific proteins in Otala lactea. Mol Cell Biochem 143 (1):15–20
Cameron RAD (1970) The survival, weight-loss and behaviour of three species of land snail in conditions of low humidity. J Zool, London 160:143–157
Dastoor Z, Dreyer J (2000) Nuclear translocation and aggregate formation of heat shock cognate protein 70 (Hsc70) in oxidative stress and apoptosis. J Cell Sci 113 (Pt 16):2845–2854
Diller KR (2006) Stress protein expression kinetics. Annu Rev Biomed Eng 8:403–424
Dong Y, Miller LP, Sanders JG, Somero GN (2008) Heat-shock protein 70 (Hsp70) expression in four limpets of the genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress. Biol Bull 215 (2):173–181
Edgerly JS, Tadimalla A, Dahlhoff EP (2005) Adaptation to thermal stress in lichen-eating webspinners (Embioptera): habitat choice, domicile construction and the potential role of heat shock proteins. Func Ecol 19 255–262
Evgen'ev MB, Garbuz DG, Shilova VY, Zatsepina OG (2007) Molecular mechanisms underlying thermal adaptation of xeric animals. J Biosci 32 (3):489–499
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Ann Rev Physiol 61:243–282
Jaffe S (1988) Climate of Israel. In: Yom-Tov Y and Tchernov E (eds) The Zoogeography of Israel. Dr. W. Junk Publishers, Dordrecht, pp 79–94
Köhler HR, Lazzara R, Dittbrenner N, Capowiez Y, Mazzia C, Triebskorn R (2009) Snail phenotypic variation and stress proteins: do different heat response strategies contribute to Waddington's widget in field populations? J Exp Zool B Mol Dev Evol 312 (2):136–147
Kotoglou P, Kalaitzakis A, Vezyraki P, Tzavaras T, Michalis LK, Dantzer F, Jung JU, Angelidis C (2009) Hsp70 translocates to the nuclei and nucleoli, binds to XRCC1 and PARP-1, and protects HeLa cells from single-strand DNA breaks. Cell Stress Chaperones 14 (4):391–406
Krebs RA, Bettencourt BR (1999) Evolution of thermotolerance and variation in the heat shock protein, Hsp70. Amer Zool 39:910–919
Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress and Chaperones 2 (1):60–71
Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92 (5):2177–2186
Lindquist S (1986) The heat-shock response. Ann Rev Biochem 55:1151–1191
Lindquist S, Craig EA (1988) The heat-shock proteins. Ann Rev Gen 22:631–677
Machin J (1967) Structural adaptation for reducing water-loss in three species of terrestrial snails. J Zool, London 152:55–65
Mizrahi T, Heller J, Goldenberg S, Arad Z (2010) Heat shock proteins and resistance to desiccation in congeneric land snails. Cell Stress and Chaperones 15:351–363. doi:10.1007/s12192-009-0150-9
Mizrahi T, Heller J, Goldenberg S, Arad Z (2011) Heat shock protein expression in relation to reproductive cycle in land snails: Implications for survival. Comp Biochem Physiol A Mol Integr Physiol 160 (2):149–155
Nakano K, Iwama G (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 (1):79–94
Pakay JL, Withers PC, Hobbs AA, Guppy M (2002) In vivo downregulation of protein synthesis in the snail Helix apersa during estivation. Amer J Physiol 283 (1):R197-204
Ramnanan CJ, Allan ME, Groom AG, Storey KB (2009) Regulation of global protein translation and protein degradation in aerobic dormancy. Mol Cell Biochem 323 (1–2):9–20
Reuner A, Brümmer F, Schill RO (2008) Heat shock proteins (Hsp70) and water content in the estivating Mediterranean Grunt Snail (Cantareus apertus). Comp Biochem Physiol B 151 (1):28–31
Scheil AE, Köhler HR, Triebskorn R (2011) Heat tolerance and recovery in Mediterranean land snails after pre-exposure in the field. J Molluscan studies 77:165–174
Schmidt-Nielsen K, Taylor CR, Shkolnik A (1971) Desert snails: problems of heat, water and food. J Exp Biol 55:385–398
Schmidt-Nielsen K, Taylor CR, Shkolnik A (1972) Desert snail: problems of survival Symp Zool Soc Lond 31:1–13
Shabtay A, Arad Z (2005) Ectothermy and endothermy: evolutionary perspectives of thermoprotection by HSPs. J Exp Biol 208 (Pt 14):2773–2781
Somero GN (1995) Proteins and temperature. Ann Rev Physiol 57:43–68
Sørensen JG, Michalak P, Justesen J, Loeschcke V (1999) Expression of the heat-shock protein HSP70 in Drosophila buzzatii lines selected for thermal resistance. Hereditas 131 (2):155–164
Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037
Storey KB (2002) Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol A 133 (3):733–754
Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202 (Pt 21):2925–2936
Wang S, Xie W, Rylander MN, Tucker PW, Aggarwal S, Diller KR (2008) HSP70 kinetics study by continuous observation of HSP-GFP fusion protein expression on a perfusion heating stage. Biotechnol Bioeng 99 (1):146–154
Acknowledgments
We thank Dr. Carmi Korine for his assistance in desert snail collection. This work was supported by the Israel Science Foundation grant.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mizrahi, T., Heller, J., Goldenberg, S. et al. The heat shock response in congeneric land snails (Sphincterochila) from different habitats. Cell Stress and Chaperones 17, 639–645 (2012). https://doi.org/10.1007/s12192-012-0340-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-012-0340-8