Comprehensive transcriptome analysis unravels the perturbated cardiovascular-related molecular mechanisms of tilapia under high-temperature stress

Abstract

With the ongoing intensification of global warming, thermal stress poses significant challenges to tilapia aquaculture. However, the molecular mechanisms underlying the cardiac response of tilapia to high temperatures remain largely unexplored. To address this knowledge gap, we investigated the effects of high-temperature stress on the transcriptomic landscape of the tilapia heart. RNA sequencing was performed on the hearts of Oreochromis aureus (AR), Oreochromis niloticus (NL), and hybrids (O. niloticus ♀ × O. aureus ♂, AN) under treatments of 28 °C, 36 °C, and 39 °C. Using a multi-method approach, including Differentially Expressed Genes analysis, Weighted Gene Co-expression Network Analysis, Fuzzy C-Means, Self-Organizing Map, and Support Vector Machine-Recursive Feature Elimination, we identified six marker genes at 39 °C (AR: ptges3, tuba1a; NL: ran, tcima; AN: slc16a1, fam184b). These genes exhibited strong positive correlations and increased expression under high-temperature conditions. Gene Set Enrichment Analysis and GENIE3 revealed that these marker genes closely regulate three cardiovascular-related pathways: adrenergic signaling in cardiomyocytes, vascular smooth muscle contraction, and cardiac muscle contraction. We hypothesize that the synergistic inhibition of these pathways by marker genes leads to the deterioration of cardiovascular function. In summary, thermal stress activates marker genes, which in turn inhibit cardiovascular pathways, impairing cardiac performance. We propose that these marker genes could serve as dynamic thermal indicators of cardiac performance in tilapia. Additionally, our findings provide theoretical support for improving the management of tilapia farming under high-temperature stress.