Heat shock proteins and resistance to desiccation in congeneric land snails

Abstract

Land snails are subject to daily and seasonal variations in temperature and in water availability and depend on a range of behavioral and physiological adaptations for coping with problems of maintaining water, ionic, and thermal balance. Heat shock proteins (HSPs) are a multigene family of proteins whose expression is induced by a variety of stress agents. We used experimental desiccation to test whether adaptation to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desiccation-resistant, desert species Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species Sphincterochila cariosa. We examined the HSP response in the foot, hepatopancreas, and kidney tissues of snails exposed to normothermic desiccation. Our findings show variations in the HSP response in both timing and magnitude between the two species. The levels of endogenous Hsp72 in S. cariosa were higher in all the examined tissues, and the induction of Hsp72, Hsp74, and Hsp90 developed earlier than in S. zonata. In contrary, the induction of sHSPs (Hsp25 and Hsp30) was more pronounced in S. zonata compared to S. cariosa. Our results suggest that land snails use HSPs as part of their survival strategy during desiccation and as important components of the aestivation mechanism in the transition from activity to dormancy. Our study underscores the distinct strategy of HSP expression in response to desiccation, namely the delayed induction of Hsp70 and Hsp90 together with enhanced induction of sHSPs in the desert-dwelling species, and suggests that evolution in harsh environments will result in selection for reduced Hsp70 expression.

Natural annual cycle of heat shock protein expression in land snails: desertversusMediterranean species ofSphincterochila

“…The authors concluded that Hsp70 does not have an essential function during aestivation in this species except for possible basal metabolic activities, and that the upregulation of HSPs in aestivating O. lacteal, as demonstrated by Brooks and Storey (Brooks and Storey, 1995), might be limited to the transition from an active to a depressed state, and might be not apparent in animals in the dormant state. This suggestion is confirmed by our studies in the land snail Sphincterochila, which provide a wider insight into the aestivation process, indicating the involvement of the HSP machinery in both experimental desiccation and as part of the natural annual cycle of activity and aestivation (Mizrahi et al, 2010) (present study). However, in contrast to experimental desiccation, in which desiccation induced the expression of most tested HSPs (Mizrahi et al, 2010), there was a general downregulation of HSP levels in aestivating compared with in active snails.…”

“…The authors concluded that, in Artemia, this protein might play the role of a metabolic regulator and/or a protective molecular chaperone during prolonged anoxia and other forms of stress. Our finding that sHSP responses were more pronounced in S. zonata compared with in S. cariosa is in agreement with our previous study demonstrating the stronger response of sHSPs to experimental desiccation in S. zonata snails (Mizrahi et al, 2010). However, it seems that the weaker induction of sHSPs in S. cariosa snails might reflect the higher standing stocks of sHSPs in this species that might suffice upon arousal.…”

“…Recently, our study in the land snail Sphincterochila revealed a general induction of various HSPs (members of the 70kDa, 90kDa and sHSPs families) in response to experimental desiccation in a species-and tissue-dependent manner (Mizrahi et al, 2010). These findings suggest that land snails use HSPs as part of their survival strategy during desiccation, and as important components of the aestivation mechanism in the transition from activity to dormancy.…”

“…The present study aimed to test whether the natural annual activity cycle of land snails involves the stress protein machinery and, if so, whether desert species differ from their non-desert congeners in their strategies, as recently suggested by Mizrahi et al (Mizrahi et al, 2010) for Sphincterochila. We thus sampled S. zonata and S. cariosa in their respective desert and Mediterranean habitats during aestivation and arousal, and analyzed several tissues for various HSPs.…”

“…Our recent study (Mizrahi et al, 2010) suggested that Sphincterochila species that differ in their resistance to experimental desiccation developed distinct strategies of HSP expression that reflect the difference in aridity encountered in their natural habitats. The desert inhabiting, desiccation-resistant S. zonata, which is naturally exposed to extreme environmental conditions, maintained lower standing stocks of Hsp70 under normal conditions compared with the Mediterranean-type, desiccation-sensitive species S. cariosa.…”