Physiological and transcriptomic responses in brown trout, Salmo trutta, to multiple stressors: Pesticide mixtures, elevated water temperature and the proliferative kidney disease

Contamination with pesticides, rising water temperatures and pathogen pressure represent a multiple stressor scenario relevant to surface water ecosystems globally. This study investigated the combination of three environmental stressors on juvenile brown trout, Salmo trutta. Fish acclimatised to either 12 or 15 °C, were exposed for 14 days to one (at 12 °C) or two (at 15 °C) sublethal concentrations of a pesticide mixture (fluopyram, epoxiconazole, diuron, chlorpyrifos, λ-cyhalothrin), then were maintained in clean water for three months, with half exposed to T. bryosalmonae, the causative agent of proliferative kidney disease (PKD). Pesticide exposure alone neither caused mortality nor changes in growth, hematocrit, or organ indices. However, the transcriptome (RNA-Seq) and gene expression (RT-qPCR) in brain and liver were significantly altered. No interactions between temperature and pesticide exposure were observed on apical, physiological, or qPCR endpoints and susceptibility to PKD was not affected by pesticide exposure. However, transcriptomic analysis revealed that the number of differentially expressed genes (DEGs) induced by pesticides was greater at 15 °C. Moreover, the number of DEGs affected by temperature in the brain was strongly reduced in the presence of pesticides. In addition, fish exhibited decreased basal oxygen consumption 2.5 months after exposure to the higher pesticide concentration at 15 °C suggesting potential metabolic trade-offs. Overall, our findings emphasize the need for ecotoxicological studies to incorporate multi-stressor scenarios and the importance of considering sublethal effects in understanding the response of fish populations to pesticide contamination in a changing climate.