Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect

Abstract

Antarctica's terrestrial environment is a challenge to which very few animals have adapted. The largest, free-living animal to inhabit the continent year-round is a flightless midge, Belgica antarctica. Larval midges survive the lengthy austral winter encased in ice, and when the ice melts in summer, the larvae complete their 2-yr life cycle, and the wingless adults form mating aggregations while subjected to surprisingly high substrate temperatures. Here we report a dichotomy in survival strategies exploited by this insect at different stages of its life cycle. Larvae constitutively up-regulate their heat shock proteins (small hsp, hsp70, and hsp90) and maintain a high inherent tolerance to temperature stress. High or low temperature exposure does not further upregulate these genes nor does it further enhance thermotolerance. Such ''preemptive'' synthesis of hsps is sufficient to prevent irreversible protein aggregation in response to a variety of common environmental stresses. Conversely, adults exhibit no constitutive up-regulation of their hsps and have a lower intrinsic tolerance to high temperatures, but their hsps can be thermally activated, resulting in enhanced thermotolerance. Thus, the midge larvae, but not the adults, have adopted the unusual strategy of expressing hsps continuously, possibly to facilitate proper protein folding in a cold habitat that is more thermally stable than that of the adults but a habitat subjected frequently to freeze-thaw episodes and bouts of pH, anoxic, and osmotic stress.Antarctica ͉ cold tolerance ͉ protein aggregation ͉ temperature stress ͉ thermotolerance

Up-regulation of heat shock proteins is essential for cold survival during insect diapause

“…Hsp expression is strongly up-regulated during dormancies ranging from encystment in the brine shrimp, Artemia franciscana (33), and the quiescent stages of the freshwater sponge, Spongilla lacustris (34), to mammalian hibernation (35,36), and small Hsps are up-regulated during dormancy in a number of plant tissues including seeds (37-39), parenchyma cells (40), and bark tissue (41). Additionally, polar organisms including larvae of the terrestrial Antarctic midge, Belgica antarctica (42), an Antarctic fish, Trematomus bernacchii, (43), and an Antarctic marine ciliate, Euplotes focardii (44), continuously express Hsps. Thus, Hsps appear to be widely used by organisms subjected to cold environments.…”

Heat shock protein expression enhances heat tolerance of reptile embryos

“…R. Soc. B 281: 20141135 stress: for example, some maintain a high constitutive level of HSP70 rather than enhancing the expression of inducible HSP70 [39,41,[45][46][47]. Accordingly, the big difference in the expression of the hsp70 gene between bird and reptile embryos may not necessary reflect the difference in heat tolerance between the two lineages (figure 1).…”

How insects survive the cold: molecular mechanisms—a review

“…An interesting twist to the use of HSPs as a protective cellular mechanism in cold shock is provided by the work of Rinehart et al (2006b). Their studies on the Antarctic flightless midge Belgica antarctica show continuous up-regulation of HSPs (Hsp70, Hsp90 and smHsp) in larvae, but not the adult stages, with the latter displaying the classical activation patterns in response to both high and low temperatures.…”

“…Therefore, the adults need protection against high, as well as low temperatures and the inducible mechanism is clearly the most energetically efficient way to achieve this. Conversely, the larvae, with their restricted stable temperature regime are in a situation akin to the Antarctic marine organisms and in this case the constitutive expression can be seen as a common adaptation to the Antarctic environment, with a strong requirement for facilitating proper folding of proteins at low temperatures (Rinehart et al 2006b;Place et al 2004;Clark et al 2008). …”