The effect of cold acclimation on active ion transport in cricket ionoregulatory tissues

Abstract

Cold-acclimated insects defend ion and water transport function during cold exposure. We hypothesized that this is achieved via enhanced active transport. The Malpighian tubules and rectum are likely targets for such transport modifications, and recent transcriptomic studies indicate shifts in Na-K ATPase (NKA) and V-ATPase expression in these tissues following cold acclimation. Here we quantify the effect of cold acclimation (one week at 12°C) on active transport in the ionoregulatory organs of adult Gryllus pennsylvanicus field crickets. We compared primary urine production of warm- and cold-acclimated crickets in excised Malpighian tubules via Ramsay assay at a range of temperatures between 4 and 25°C. We then compared NKA and V-ATPase activities in Malpighian tubule and rectal homogenates from warm- and cold-acclimated crickets via NADH-linked photometric assays. Malpighian tubules of cold-acclimated crickets excreted fluid at lower rates at all temperatures compared to warm-acclimated crickets. This reduction in Malpighian tubule excretion rates may be attributed to increased NKA activity that we observed for cold-acclimated crickets, but V-ATPase activity was unchanged. Cold acclimation had no effect on rectal NKA activity at either 21°C or 6°C, and did not modify rectal V-ATPase activity. Our results suggest that an overall reduction, rather than enhancement of active transport in the Malpighian tubules allows crickets to maintain hemolymph water balance during cold exposure, and increased Malpighian tubule NKA activity may help to defend and/or re-establish ion homeostasis.

Functional plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia inDrosophila melanogaster

“…These results are also informative in that they show that the Malpighian tubules are more temperature sensitive than the rectum and exhibit a greater degree of adjustment to K + transport following cold acclimation both in terms of thermal sensitivity and in absolute K + transport rates. This supports the idea that reduced Malpighian tubule K + clearance is a central problem for D. melanogaster at low temperatures, as is the case for crickets (Des Marteaux et al, 2018), and that its preservation is thus beneficial to the development of chill tolerance. The effects of cold acclimation on ion transport are independent of V-type H + -ATPase and Na + /K + -ATPase activity…”

“…Thus chill tolerance in coldadapted and -acclimated flies appears to be at least partially improved by improved tubule K + secretion at low temperature. In addition, in contrast to the tubule fluid secretion in CA D. melanogaster, a recent study on CA crickets found reduced fluid secretion rates at lower temperatures, suggesting that a different mechanism exists in the cold acclimation of these two insects (Des Marteaux et al, 2018).…”

“…To date, differences in ionoregulatory organ function that relate to cold tolerance have only been described in the Malpighian tubules and rectal pads among Drosophila species that differ in chill tolerance (MacMillan et al, 2015d;Andersen et al, 2017b) and in the Malpighian tubules of cold-acclimated Gryllus pennsylvanicus (Des Marteaux et al, 2018). Whereas low temperatures disturbed the ratio of Na + :K + secreted by the tubules of chill-susceptible Drosophila species, tolerant species experience little or no such change (MacMillan et al, 2015d).…”

“…Conversely, in absorptive tissues such as the hindgut and the Malpighian tubules, reductions of ion-motive ATPases would reduce ion absorption and thus mitigate the active re-uptake of K + in the cold. To date, whole body Na + /K + -ATPase activity has been measured in coldacclimated Drosophila (MacMillan et al, 2015b) and an organspecific assessment of Na + /K + -ATPase and V-type H + -ATPase activity in cold-acclimated G. pennsylvanicus has been conducted (Des Marteaux et al, 2018). In the present study, a complete assessment of both organ-specific Na + /K + -ATPase and V-type H + -ATPase activities alongside functional measurements for the midgut, the Malpighian tubules and the hindgut are presented for D. melanogaster.…”

Cold stress results in sustained locomotor and behavioral deficits in Drosophila melanogaster

“…As the seasons change from autumn to winter, insects use environmental cues such as day length and gradual decrease in temperature to sense the onset of winter and trigger physiological changes (Teets & Denlinger, ). Gradual climatic transitions provide insects the opportunity to acclimate to cold conditions (Jakobs, Gariepy, & Sinclair, ; Sinclair, Coello Alvarado, & Ferguson, ; Teets & Denlinger, ), and indeed cold acclimation directly impacts osmotic regulation to preserve ion homeostasis at low temperature (e.g., Andersen et al, ; Des Marteaux et al, ; MacMillan, Yerushalmi, Jonusaite, Kelly, & Donini, ). In D. melanogaster male reproductive behaviors are negatively influenced by severe cold exposure (Singh & Prasad, ), but exposure to brief cold acclimation (i.e., rapid cold hardening) preserves male reproductive behavior and success (Shreve et al, ).…”