Thermal stress induces tissue damage and a broad shift in regenerative signaling pathways in the honey bee digestive tract

Abstract

Honey bee colonies in the United States have suffered from increased die-off in the last few years with a complex set of interacting stresses playing a key role. With changing climate, an increase in the frequency of severe weather events, such as heat waves, is anticipated. Understanding how these changes may contribute to stress in honey bees is crucial. Individual honey bees appear to have a high capacity to endure thermal stress. One reason for this high-level endurance is likely their robust HSR which contributes to thermotolerance at the cellular level. However, less is known about other mechanisms of thermotolerance, especially those operating at the tissue level. To elucidate other determinants of this resilience in this species, we used thermal stress coupled with RNAseq and identified broad transcriptional remodeling of a number of key signaling pathways in the honey bee, including those pathways known to be involved in digestive tract regeneration in the fruit fly such as the Hippo and JAK/STAT pathways. We also observe cell death and shedding of epithelial cells, which likely leads to induction of this regenerative transcriptional program. We found that thermal stress affects many of these pathways in other tissues, suggesting a shared program of damage response. This study provides important foundational characterization of the tissue damage response program in this key pollinating species. In addition, our data suggest that a robust regeneration program may also be a critical contributor to thermotolerance at the tissue level, a possibility which warrants further exploration in this and other species.

Paromomycin Reduces Vairimorpha (Nosema) ceranae Infection in Honey Bees but Perturbs Microbiome Levels and Midgut Cell Function

“…Second, paromomycintreated cells could be so damaged that they are dying before the parasite life cycle is completed. The sloughing of midgut epithelial cells can be observed in honey bees after exposure to other stressors [57]. Third, translation inhibition in the host cells may preferentially reduce the amount of one or more specific host proteins that are necessary for optimal parasite function.…”

Differential Expression Characterisation of the Heat Shock Proteins DnaJB6, DnaJshv, DnaJB13, and DnaJB14 in Apis cerana cerana Under Various Stress Conditions

“…It has been shown that 50% or more of the sperm stored in live queen spermathecae are killed when the temperature exceeds 40 • C (Pettis et al, 2016). Recent studies have demonstrated that heat stress during development influences honey bee immunocompetence (Medina et al, 2020), and thermal stress causes a regenerative signalling pathway shift and tissue damage in bees (Bach et al, 2021). Therefore, the upregulation of DnaJBs may play crucial roles in helping bees reduce the adverse effects of heat stress.…”

Honey bee sHSP are responsive to diverse proteostatic stresses and potentially promising biomarkers of honey bee stress

“…For RNA-Seq analysis, we used data sets generated previously 6 – 8 . Briefly, we performed transcriptome profiling (RNASeq) on midguts from bees: (1) fed sucrose solution containing 24 μM Tunicamycin or DMSO for 24 h 6 , (2) maintained at either 35 or 45 °C for 4 h 7 , or (3) treated with sucrose solution containing 200 µM halofuginone or DMSO for 24 h 8 . RNASeq analysis was performed on 3 midguts from each group individually.…”

“…We used tunicamycin, which disrupts N -glycosylation in the ER to induce the UPR 6 . We also used thermal stress which causes protein denaturation and found that this induces a tissue regeneration program 7 . Finally, we used halofuginone, which inhibits the prolyl-tRNA synthetase to induce ISR, and observed increased expression of ribosome biogenesis genes 8 .…”