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

Abstract

At low temperatures, , like most insects, lose the ability to regulate ion and water balance across the gut epithelia, which can lead to a lethal increase of [K] in the hemolymph (hyperkalemia). Cold acclimation, the physiological response to a prior low temperature exposure, can mitigate or entirely prevent these ion imbalances, but the physiological mechanisms that facilitate this process are not well understood. Here, we test whether plasticity in the ionoregulatory physiology of the gut and Malpighian tubules of may aid in preserving ion homeostasis in the cold. Upon adult emergence, females were subjected to 7 days at warm (25°C) or cold (10°C) acclimation conditions. The cold-acclimated flies had a lower critical thermal minimum (CT), recovered from chill coma more quickly, and better maintained hemolymph K balance in the cold. The improvements in chill tolerance coincided with increased Malpighian tubule fluid secretion and better maintenance of K secretion rates in the cold, as well as reduced rectal K reabsorption in cold-acclimated flies. To test whether modulation of ion-motive ATPases, the main drivers of epithelial transport in the alimentary canal, mediate these changes, we measured the activities of Na/K-ATPase and V-type H-ATPase at the Malpighian tubules, midgut, and hindgut. Na/K-ATPase and V-type H-ATPase activities were lower in the midgut and the Malpighian tubules of cold-acclimated flies, but unchanged in the hindgut of cold-acclimated flies, and were not predictive of the observed alterations in K transport. Our results suggest that modification of Malpighian tubule and gut ion and water transport probably prevents cold-induced hyperkalemia in cold-acclimated flies, and that this process is not directly related to the activities of the main drivers of ion transport in these organs, Na/K- and V-type H-ATPases.

An impressive capacity for cold tolerance plasticity protects against ionoregulatory collapse in the disease vector,Aedes aegypti

“…In such cases, hyperkalemia is mitigated (at least in part) through modifications to renal ion and water transport that help to clear excess K + ions from the hemolymph and maintain hemolymph volume (M. K. Andersen, Folkersen, et al, 2017; MacMillan, Andersen, Loeschcke, et al, 2015; Yerushalmi, Misyura, MacMillan, & Donini, 2018). Although at present it is unclear whether the same mechanisms underlie improvements in chilling tolerance in mosquito larvae, the prevention of hyperkalemia likely attenuates cold-induced cell membrane depolarization, which would limit cell death and thereby facilitate survival (M.…”

Dissecting cause from consequence: a systematic approach to thermal limits

“…Dupoué et al, 2013;MacMillan et al, 2018 Urinary Failure of osmoregulatory organs or impaired clearance of ions or nitrogenous waste, leading to systemic loss of osmotic balance or accumulation of toxins. Yerushalmi et al, 2018 Reproductive Impaired egg/sperm production leading to a failure to reproduce, egg necrosis leading to infection. Brante et al, 2003;Donelson et al, 2014;Marshall and Sinclair, 2010 Immune Decreased immune function leading to an inability to effectively combat pathogens and parasites.…”

Examining the Effects of Cold on Gut Epithelial Permeability in Locusta migratoria

“…From the foregut, food travels to reach the remainder of the gut to be digested (Engel and Moran, 2013;Naikkhwah and O'Donnell, 2012). Cells along the midgut (region following the foregut) are actively involved in digestive enzyme production and secretion, acting as the primary site of digestion and nutrient, ion, and water absorption (Chapman, 2013;Yerushalmi et al, 2018). Following the midgut are the MTs, blind-ended tube-shaped diverticula of the gut that are somewhat analogous to the vertebrate kidneys (Chapman, 2013).…”

“…V-ATPase, the proton pump that primarily energizes transport at the MTs) and channels, ions such as K + , Na + and Clare driven from the hemolymph to the tubule lumen. For instance, K + is secreted into the tubule lumen which helps to maintain a low K + (generally 10-15 mM) environment where nerves and muscles can function (Andersen et al, 2017a;Andersen et al, 2018;Gerber and Overgaard, 2018;Yerushalmi et al, 2018). These means of ionoregulation across the MTs promote an osmotic gradient that favours the movement of water and unwanted waste products or toxins into the tubule lumen (secretion), producing primary urine .…”

“…Through the continuous ionoregulatory actions of the alimentary canal, the hemolymph of most insects contains high and low concentrations of Na + and K + , respectively, at optimal or near-optimal thermal conditions (Engel and Moran, 2013;. In cold conditions, however, the activity of ionoregulatory enzymes like V-ATPases and Na + /K + -ATPases is suppressed (Bayley et al, 2018;Hosler et al, 2000;Mandel et al, 1980;McMullen and Storey, 2008;Moriyama and Nelson, 1989;Yerushalmi et al, 2018).…”