An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans

Abstract

Protection of poikilothermic animals from seasonal cold is widely regarded as being causally linked to changes in the unsaturation of membrane phospholipids, yet in animals this proposition remains formally untested. We have now achieved this by the genetic manipulation of lipid biosynthesis of Caenorhabditis elegans independent of temperature. Worms transferred from 25°C to 10°C develop over several days a much-increased tolerance of lethal cold (0°C) and also an increased phospholipid unsaturation, as in higher animal models. Of the three C. elegans ⌬9-desaturases, transcript levels of fat-7 only were up-regulated by cold transfer. RNAi suppression of fat-7 caused the induction of fat-5 desaturase, so to control desaturase expression we combined RNAi of fat-7 with a fat-5 knockout. These fat-5/fat-7 manipulated worms displayed the expected negative linear relationship between lipid saturation and cold tolerance at 0°C, an outcome confirmed by dietary rescue. However, this change in lipid saturation explains just 16% of the observed difference between cold tolerance of animals held at 25°C and 10°C. Thus, although the manipulated lipid saturation affects the tolerable thermal window, and altered ⌬9-desaturase expression accounts for cold-induced lipid adjustments, the effect is relatively small and none of the lipid manipulations were sufficient to convert worms between fully cold-sensitive and fully cold-tolerant states. Critically, transfer of 10°C-acclimated worms back to 25°C led to them restoring the usual cold-sensitive phenotype within 24 h despite retaining a lipid profile characteristic of 10°C worms. Other nonlipid mechanisms of acquired cold protection clearly dominate inducible cold tolerance.⌬9-acyl desaturase ͉ lipid composition ͉ RNAi

Hyperprolinemic larvae of the drosophilid fly, Chymomyza costata , survive cryopreservation in liquid nitrogen

“…This strong effect of proline was unexpected because the cold tolerance of insects is considered a highly complex adaptive trait that is composed of numerous mechanisms (40). Individual mechanisms may interact and affect each other, making it difficult to assess their separate contributions (41). In our experiments, the entrance into diapause was a second factor that markedly improved larval freeze tolerance.…”

Phenotypic plasticity of thermal tolerance contributes to the invasion potential of Mediterranean fruit flies (Ceratitis capitata)

“…However, high and low temperature could be different stressors, and it has been argued that the mechanisms for high and low temperature tolerance may be fundamentally different (Hoffmann et al, 2003; but see discussions in Chown & Nicolson, 2004;Sinclair & Roberts, 2005). There may be some overlap in these mechanisms, for example through HSP production and membrane phospholipid composition changes (Murray et al, 2007;MacMillan et al, 2009a), and clearly inhibition of apoptosis occurs (Yi et al., 2007), although HSP production and membrane lipid remodelling may not explain the short-term survival increase conferred by RCH (MacMillan et al, 2009b). Regardless, the cross-tolerance observed in this study could translate to a survival advantage for C. capitata relative to C. rosa, as the former species can likely respond not only to low temperatures but also to increasing temperature variation.…”

Induced cold tolerance mechanisms depend on duration of acclimation in the chill sensitiveFolsomia candida(Collembola)

“…Another enzyme, ∆ 9 desaturase, can synthesize oleic acid (18:1) from desaturation of stearic acid (18:0). The relationship between ∆ 9 desaturase activity and low temperature has been well studied in fish and nematodes (Tiku et al, 1996;Murray et al, 2007). However, ∆ 9 desaturase has not previously been related to low temperature physiology in arthropods.…”