Early developmental exposure to heat shock altered the response to handling stress but had limited impacts on the susceptibility to the bacterial pathogen Yersinia ruckeri in juvenile rainbow trout (Oncorhynchus mykiss)
Rob J. McFarling , Mickael Teixeira Alves , Ellen Blaker , Lyndsay Christie , Claire Joiner , Ronny van Aerle , Eduarda M. Santos , Ioanna Katsiadaki
{"title":"Early developmental exposure to heat shock altered the response to handling stress but had limited impacts on the susceptibility to the bacterial pathogen Yersinia ruckeri in juvenile rainbow trout (Oncorhynchus mykiss)","authors":"Rob J. McFarling , Mickael Teixeira Alves , Ellen Blaker , Lyndsay Christie , Claire Joiner , Ronny van Aerle , Eduarda M. Santos , Ioanna Katsiadaki","doi":"10.1016/j.aquaculture.2025.742244","DOIUrl":null,"url":null,"abstract":"<div><div>Disease is a major limiting factor for aquaculture production, having significant implications for production as well as fish welfare, hence, novel, preferably drug-free approaches for preventing and alleviating these impacts are required. Exposure of fish to heat shock during early embryo development has the potential to alter responses to stress in later life. Due to crosstalk between thermal stress and immune signalling pathways and encouraged by the well-documented ability for elevated temperatures to influence immune function, we hypothesised that heat shock during early developmental life stages could influence responses and survival during infection. To test this hypothesis, rainbow trout embryos were heat shocked (18 °C for one hour, initiated at 19 h post fertilisation), whilst naïve controls were maintained at 10 °C. Following hatching and development, juvenile fish from both groups were challenged with the bacterial pathogen <em>Yersinia ruckeri,</em> or mock challenged (exposed to handling stress associated with the procedure) in parallel. No significant difference in survival following infection was observed between naïve and heat shocked fish (log-rank test, <em>p</em> = 0.7). Interrogation of hepatic transcription prior to infection revealed minimal differences between naïve and heat shocked fish. However, comparing the response of naïve and heat shocked fish to handling stress associated with the mock challenge revealed substantial differences in hepatic transcription. Enriched pathways including unfolded protein response, apoptosis, metabolism, oxidative stress and DNA damage, showed that the embryonic exposure to heat shock modified the response to subsequent handling stress. In contrast, naïve and heat shocked fish exposed to <em>Y. ruckeri</em> displayed minor differences in transcriptomic responses, and no alterations in pathogen-challenge survival.</div><div>Overall, our data demonstrate the potential for developmental heat shock exposure to condition the response of fish to subsequent stressors, particularly to handling stress. Further work is required to build on these findings and determine the potential for developmental heat shock as a management tool to alleviate the adverse effects of exposure to stressors in aquaculture.</div></div>","PeriodicalId":8375,"journal":{"name":"Aquaculture","volume":"600 ","pages":"Article 742244"},"PeriodicalIF":3.9000,"publicationDate":"2025-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Aquaculture","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0044848625001309","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"FISHERIES","Score":null,"Total":0}
引用次数: 0
Abstract
Disease is a major limiting factor for aquaculture production, having significant implications for production as well as fish welfare, hence, novel, preferably drug-free approaches for preventing and alleviating these impacts are required. Exposure of fish to heat shock during early embryo development has the potential to alter responses to stress in later life. Due to crosstalk between thermal stress and immune signalling pathways and encouraged by the well-documented ability for elevated temperatures to influence immune function, we hypothesised that heat shock during early developmental life stages could influence responses and survival during infection. To test this hypothesis, rainbow trout embryos were heat shocked (18 °C for one hour, initiated at 19 h post fertilisation), whilst naïve controls were maintained at 10 °C. Following hatching and development, juvenile fish from both groups were challenged with the bacterial pathogen Yersinia ruckeri, or mock challenged (exposed to handling stress associated with the procedure) in parallel. No significant difference in survival following infection was observed between naïve and heat shocked fish (log-rank test, p = 0.7). Interrogation of hepatic transcription prior to infection revealed minimal differences between naïve and heat shocked fish. However, comparing the response of naïve and heat shocked fish to handling stress associated with the mock challenge revealed substantial differences in hepatic transcription. Enriched pathways including unfolded protein response, apoptosis, metabolism, oxidative stress and DNA damage, showed that the embryonic exposure to heat shock modified the response to subsequent handling stress. In contrast, naïve and heat shocked fish exposed to Y. ruckeri displayed minor differences in transcriptomic responses, and no alterations in pathogen-challenge survival.
Overall, our data demonstrate the potential for developmental heat shock exposure to condition the response of fish to subsequent stressors, particularly to handling stress. Further work is required to build on these findings and determine the potential for developmental heat shock as a management tool to alleviate the adverse effects of exposure to stressors in aquaculture.
期刊介绍:
Aquaculture is an international journal for the exploration, improvement and management of all freshwater and marine food resources. It publishes novel and innovative research of world-wide interest on farming of aquatic organisms, which includes finfish, mollusks, crustaceans and aquatic plants for human consumption. Research on ornamentals is not a focus of the Journal. Aquaculture only publishes papers with a clear relevance to improving aquaculture practices or a potential application.