Chilling induces unidirectional solute leak through the locust gut epithelia

Chill-susceptible insects, like the migratory locust, often die when exposed to low temperatures from an accumulation of tissue damage that is unrelated to freezing (chilling injuries). Chilling injury is consistently associated with ion imbalance across the gut epithelia. It has recently been suggested that this imbalance is at least partly caused by a cold-induced disruption of epithelial barrier function. Here, we aim to test this hypothesis in the migratory locust ( L. migratoria ). First, chill tolerance was quantified by exposing locusts to −2°C for various durations and monitored for chill coma recovery time and survival 24h post-cold exposure. Longer exposure times significantly increased recovery time and caused injury and death. Ion-selective microelectrodes were also used to determine the presence of cold-induced ion imbalance. We found a significant increase and decrease of hemolymph K + and Na + concentrations over time, respectively. Next, barrier failure along the gut was tested by monitoring the movement of an epithelial barrier marker (FITC-dextran) across the gut epithelia during exposure to −2°C. We found minimal marker movement across the epithelia in the serosal to mucosal direction, suggesting that locust gut barrier function remains generally conserved during chilling. However, when tested in the mucosal to serosal direction, we saw significant increases of FITC-dextran with chilling. This instead suggests that while cold-induced barrier disruption is present, it is likely unidirectional. It is important to note that these data reveal only the phenomenon itself. The location of this leak as well as the underlying mechanisms remain unclear and require further investigation. Summary statement In this study, we provide the first evidence for the presence of cold-induced paracellular leak along the gut of the migratory locust, and that this leak is strongest in the mucosal to serosal direction.