Multi-Omics Analysis Provides Novel Insight into Immuno-Physiological Pathways and Development of Thermal Resistance in Rainbow Trout Exposed to Acute Thermal Stress

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.

Effect of Temperature Fluctuation and Nutritional Status on Starry Flounder, Platichthys stellatus, Survival and Adaptive Physiological Response

“…GPT and GOT levels increased rapidly in rainbow trout after they were exposed to acute thermal stress as reported by Roh et al [41]. In the present study, levels of GPT and GOT secreted in the liver were above the detection limit (≥1000 U/L) with the increase in water temperature, and then decreased towards the end of the experiment.…”

Dual-Organ Transcriptomic Analysis of Rainbow Trout Infected With Ichthyophthirius multifiliis Through Co-Expression and Machine Learning

“…In order to validate RNA-seq, eight DEGs were selected in consideration of the biomarkers known to be meaningful for the infectious disease and/or stress environment in former studies and the pattern of transcriptomic expression in this study ( 40 , 42 , 43 ). The expression levels of some DEGs were validated using qPCR.…”

“…To validate sequence quantification, real-time PCR was performed targeting some selected DEGs (SAA, Hap, HSP70, Hmx, CD99, IgT, Wap65-1, and Col). cDNA synthesis and qPCR were performed following a previous study ( 40 ). Briefly, cDNAs were synthesized from 1 µg total RNAs.…”

Transcriptome analysis unveils survival strategies of Streptococcus parauberis against fish serum

“…Transcripts of broth-cultured samples were used as controls for the serum-cultured samples at every sampling time point. To measure gene expression profiles based on eggNOG functional categories [23], z-score was calculated by dividing the number of significantly up-and down-regulated genes (with consideration of FDR only, significance at < 1e -5 ) by the square of the total number of differentially expressed genes (DEGs) [24]. z À score ¼ ðUp regulated DEG countÞ À ðDown regulated DEG countÞ ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi ffi Total DEG count p…”