Dietary potassium and cold acclimation additively increase cold tolerance in Drosophila melanogaster

In the cold, chill susceptible insects lose the ability to regulate ionic and osmotic gradients. This leads to hemolymph hyperkalemia that drives a debilitating loss of cell membrane polarization, triggering cell death pathways and causing organismal injury. Biotic and abiotic factors can modulate insect cold tolerance by impacting the ability to mitigate or prevent this cascade of events. In the present study, we test the combined and isolated effects of dietary manipulations and thermal acclimation on cold tolerance in fruit flies. Specifically, we acclimated adult Drosophila melanogaster to 15 or 25 °C and fed them either a K⁺-loaded diet or a control diet. We then tested the ability of these flies to recover from and survive a cold exposure, as well as their capacity to protect transmembrane K⁺ gradients, and intracellular Na⁺ concentration. As predicted, cold-exposed flies experienced hemolymph hyperkalemia and cold-acclimated flies had improved cold tolerance due to an improved maintenance of the hemolymph K⁺ concentration at low temperature. Feeding on a high-K⁺ diet improved cold tolerance additively, but paradoxically reduced the ability to maintain extracellular K⁺ concentrations. Cold-acclimation and K⁺-feeding additively increased the intracellular K⁺ concentration, aiding in maintenance of the transmembrane K⁺ gradient during cold exposure despite cold-induced hemolymph hyperkalemia. There was no effect of acclimation or diet on intracellular Na⁺ concentration. These findings suggest intracellular K⁺ loading and reduced muscle membrane K⁺ sensitivity as mechanisms through which cold-acclimated and K⁺-fed flies are able to tolerate hemolymph hyperkalemia.