Proteome stability, heat hardening, and heat-shock protein expression profiles in Cataglyphis desert ants

Abstract

In ectotherms, high temperatures impose physical limits, impeding activity. Exposure to high heat levels causes various deleterious and lethal effects, including protein misfolding and denaturation. Thermophilic ectotherms have evolved various ways to increase macromolecular stability and cope with elevated body temperatures; these include the high constitutive expression of molecular chaperones. In this study, we investigated the effect of moderate to severe heat shock (37-45°C) on survival, heat hardening, protein damage and the expression of five heat tolerance-related genes (hsc70-4 h1, hsc70-4 h2, hsp83, hsc70-5 and hsf1) in two closely related Cataglyphis ants that occur in distinct habitats. Our results show that the highly thermophilic Sahara ant Cataglyphis bombycina constitutively expresses HSC70 at higher levels, but has lower induced expression of heat tolerance-related genes in response to heat shock, as compared with the more mesophilic Cataglyphis mauritanica found in the Atlas Mountains. As a result, C. bombycina demonstrates increased protein stability when exposed to acute heat stress but is less disposed to acquiring induced thermotolerance via heat hardening. These results provide further insight into the evolutionary plasticity of the hsp gene expression system and subsequent physiological adaptations in thermophilous desert insects to adapt to harsh environmental conditions.

Evidence for lower plasticity in CTMAX at warmer developmental temperatures

“…The mechanisms underpinning the hardening responses have been well defined in D. melanogaster and are linked to the upregulation of Hsp70, but changes in Hsp70 expression have not been linked to hardening in other Drosophila species (Krebs, 1999;Hoffmann et al, 2003). These results suggest that the capacity for Hsp70 to act as regulator of heat plasticity may be species-specific (Hamdoun et al, 2003;Ravaux et al, 2016;Willot et al, 2017). Despite plasticity only shifting CT MAX by <0.60°C, mechanistic species distribution models have shown that even a 0.50°C change in CT MAX can contribute to meaningful reductions in projected range losses under climate change (Bush et al, 2016).…”

“…The mechanisms underpinning the hardening responses have been well defined in D. melanogaster and are linked to the upregulation of Hsp70, but changes in Hsp70 expression have not been linked to hardening in other Drosophila species (Krebs, ; Hoffmann et al ., ). These results suggest that the capacity for Hsp70 to act as regulator of heat plasticity may be species‐specific (Hamdoun et al ., ; Ravaux et al ., ; Willot et al ., ).…”

“…Shorter exposures (minutes-hours) at more stressful temperatures are often referred to as hardening. Hardening responses in heat resistance have been extensively studied in Drosophila and are linked to the transient upregulation of heat-shock proteins (Telonis-Scott et al, 2014;Willot et al, 2017). In ectothermic species, temperature acclimation (both developmental and adult) and adult hardening treatments increase heat resistance with increasing temperature (Chown, 2001;Hoffmann et al, 2003).…”

Research Article Heat shock genes in the stingless bee <i>Melipona interrupta</i> (Hymenoptera, Meliponini)

“…Temperature is one of the most important abiotic factors regulating the activities of cold-blooded (pecilothermal) organisms, such as insects. Due to a large variety of behavioral and physiological strategies, insects have the ability to survive at different temperatures by synthetizing heat shock proteins HSPs, which are molecules that provide thermal protection (Rafael et al 2012;Lu et al, 2016;Willot et al, 2017). The HSPs are part of a highly conserved and universal group of proteins found in all organisms that have been studied.…”

“…In addition, HSPs are regulated during insect development, being up-regulated during diapause (Zhao and Jones, 2012;Shen et al, 2015). However, the most well characterized molecular responses in insects are those involving thermal shock, mainly heat stress (Lu et al, 2016;Zhang et al, 2016;Willot et al, 2017), because temperature can affect fecundity, development, growth, population abundance, survival and geographic distribution of these organisms (Paul and Keshan, 2016;Lu et al, 2016;Li et al, 2017). Temperature increase can be more harmful to tropical insects because they live close to their maximum thermal limit when compared to temperate zone insects (Evgen'ev et al, 2014;Paul and Keshan, 2016).…”