Abstract
In recent years, poikilothermic animals such as fish have increasingly been exposed to stressful high-temperature environments due to global warming. However, systemic changes in fish under thermal stress are not fully understood yet at both the transcriptome and proteome level. Therefore, the objective of this study was to investigate the immuno-physiological responses of fish under extreme thermal stress through integrated multi-omics analysis. Trout were exposed to acute thermal stress by raising water temperature from 15 to 25 °C within 30 min. Head-kidney and plasma samples were collected and used for RNA sequencing and two-dimensional gel electrophoresis. Gene enrichment analysis was performed: differentially expressed genes (DEGs) and differentially expressed proteins (DEPs) were identified to interpret the multi-omics results and identify the relevant biological processes through pathway analysis. Thousands of DEGs and 49 DEPs were identified in fish exposed to thermal stress. Most of these genes and proteins were highly linked to DNA replication, protein processing in the endoplasmic reticulum, cell signaling and structure, glycolysis activation, complement-associated hemolysis, processing of released free hemoglobin, and thrombosis and hypertension/vasoconstriction. Notably, we found that immune disorders mediated by the complement system may trigger hemolysis in thermally stressed fish, which could have serious consequences such as ferroptosis and thrombosis. However, antagonistic activities that decrease cell-free hemoglobin, heme, and iron might be involved in alleviating the side effects of thermally induced immuno-physiological disorders. These factors may represent the major thermal resistance traits that allow fish to overcome extreme thermal stress. Our findings, based on integration of multi-omics data from transcriptomics and proteomics analyses, provide novel insight into the pathogenesis of acute thermal stress and temperature-linked epizootics.
Highlights
Fish are poikilothermic animals that live in an aquatic environment
The rainbow trout used in this study appeared to be phenotypically thermal-tolerant as they all survived for two weeks without showing any signs of disease when the water temperature was increased 10 ◦C from 15 to 25 ◦C within 30 min
Thousands of differentially expressed genes (DEGs) were identified in stressed fish at 4, 24, and 72 hpt, indicating that dramatic changes occur in the transcriptome that are greater than those seen in fish under chronic thermal stress [13]
Summary
Fish are poikilothermic animals that live in an aquatic environment. Their physiological and metabolic responses are highly correlated with acclimated temperatures [1,2]. All sea bream (Sparus aurata) were killed within one week when water temperature was increased 12 ◦C at a rate of 6 ◦C day−1 [8]. In light of these trends, the importance of examining the global immuno-physiological characteristics of fish under acute thermal stress cannot be overstated. Given that contrasting transcriptomic responses might occur in response to chronic vs. acute stress in teleosts [14], identification of systemic biological responses in fish exposed to acute thermal stress would aid in understanding temperature-linked epizootics
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