Olsson Trine, MacMillan Heath A, Nyberg Nils, Staerk Dan, Malmendal Anders, Overgaard Johannes
Zoophysiology, Department of Bioscience, Aarhus University, C.F. Møllers Allé 3, Building 1131, Aarhus DK-8000, Denmark.
Department of Drug Design and Pharmacology, University of Copenhagen, Universitetsparken 2, Copenhagen O DK-2100, Denmark.
J Exp Biol. 2016 Aug 15;219(Pt 16):2504-13. doi: 10.1242/jeb.140152. Epub 2016 Jun 15.
Drosophila, like most insects, are susceptible to low temperatures, and will succumb to temperatures above the freezing point of their hemolymph. For these insects, cold exposure causes a loss of extracellular ion and water homeostasis, leading to chill injury and eventually death. Chill-tolerant species are characterized by lower hemolymph [Na(+)] than chill-susceptible species and this lowered hemolymph [Na(+)] is suggested to improve ion and water homeostasis during cold exposure. It has therefore also been hypothesized that hemolymph Na(+) is replaced by other 'cryoprotective' osmolytes in cold-tolerant species. Here, we compared the hemolymph metabolite profiles of five drosophilid species with marked differences in chill tolerance. All species were examined under 'normal' thermal conditions (i.e. 20°C) and following cold exposure (4 h at 0°C). Under benign conditions, total hemolymph osmolality was similar among all species despite chill-tolerant species having lower hemolymph [Na(+)]. Using NMR spectroscopy, we found that chill-tolerant species instead have higher levels of sugars and free amino acids in their hemolymph, including classical 'cryoprotectants' such as trehalose and proline. In addition, we found that chill-tolerant species maintain a relatively stable hemolymph osmolality and metabolite profile when exposed to cold stress while sensitive species suffer from large increases in osmolality and massive changes in their metabolic profiles during a cold stress. We suggest that the larger contribution of classical cryoprotectants in chill-tolerant Drosophila plays a non-colligative role for cold tolerance that contributes to osmotic and ion homeostasis during cold exposure and, in addition, we discuss how these comparative differences may represent an evolutionary pathway toward more extreme cold tolerance of insects.
与大多数昆虫一样，果蝇对低温敏感，在高于其血淋巴冰点的温度下会死亡。对于这些昆虫来说，低温暴露会导致细胞外离子和水平衡失调，从而导致冷损伤并最终死亡。耐寒物种的特征是血淋巴中[Na⁺]含量低于冷敏感物种，据推测，这种较低的血淋巴[Na⁺]含量有助于在低温暴露期间改善离子和水平衡。因此，也有人推测，在耐寒物种中，血淋巴中的Na⁺被其他“抗冻”渗透溶质所取代。在这里，我们比较了五种耐寒性差异显著的果蝇物种的血淋巴代谢物谱。所有物种均在“正常”热条件下（即20°C）以及低温暴露后（0°C下4小时）进行检查。在良性条件下，尽管耐寒物种的血淋巴[Na⁺]含量较低，但所有物种的血淋巴总渗透压相似。通过核磁共振光谱，我们发现耐寒物种的血淋巴中糖和游离氨基酸的含量较高，包括海藻糖和脯氨酸等经典的“抗冻剂”。此外，我们发现耐寒物种在暴露于冷应激时能保持相对稳定的血淋巴渗透压和代谢物谱，而敏感物种在冷应激期间血淋巴渗透压大幅升高，代谢谱发生巨大变化。我们认为，经典抗冻剂在耐寒果蝇中发挥的更大作用对耐寒性起到了非依数性作用，有助于在低温暴露期间维持渗透压和离子平衡，此外，我们还讨论了这些比较差异可能如何代表昆虫向更强耐寒性进化的途径。
