AUTHOR=Duan Yuting , Li Hejiao , Li Junting , Bai Shuhao , Fu Suxing , Zhou Yinhua , Liu Shidong , Li Rundong , Liu Haiping , Zhou Chaowei , Lei Luo 

TITLE=Integrated transcriptome and 16S rDNA analyses reveal that acute heat stress induces intestinal damage in Gymnocypris eckloni

JOURNAL=Frontiers in Marine Science

VOLUME=11

YEAR=2024

URL=https://www.frontiersin.org/journals/marine-science/articles/10.3389/fmars.2024.1448313

DOI=10.3389/fmars.2024.1448313

ISSN=2296-7745

ABSTRACT=<p><italic>Gymnocypris eckloni</italic> (<italic>G. eckloni</italic>), a cold-water economic fish, is widely cultivated in southwestern China. The increase in extreme summer weather conditions owing to global warming can significantly affect their survival and health. The fish intestine and its microbiota are closely associated with fish feeding and growth, nutritional metabolism, and immune defense. However, the mechanisms underlying the changes in the <italic>G. eckloni</italic> intestine and its microbiota under acute heat stress remain unknown. In this study, we investigated the effects of acute heat stress on the <italic>G. eckloni</italic> intestine employing histology, plasma biochemical indices, transcriptomics, and 16S rDNA sequencing. Histological analysis showed that acute heat stress induced significant morphological damage to the intestine, with microvilli detachment and mitochondrial abnormalities in the ultrastructure. Biochemical indicators associated with stress (reactive oxygen species and catalase), inflammation (interleukin-1β and tumor necrosis factor-α), and intestinal permeability (diamine oxidase and lipopolysaccharide) were significantly elevated after acute heat stress, indicating an intestinal inflammatory response and disruption of barrier function. Many DEGs were mined by transcriptomic analysis, with <italic>tfrc, pfkp, egln1</italic> enriched in the HlF-1 signaling pathway, <italic>hsp70, hsp90aa1</italic> and <italic>hspa4</italic> enriched in the Antigen processing and presentation pathway, <italic>pmm1</italic>, <italic>pfkfb3</italic> and <italic>hk1</italic> enriched in the Fructose and mannose metabolism patyway. The HIF-1 signaling pathway is a crucial regulatory pathway during acute heat stress in the <italic>G. eckloni</italic> intestine, while significant downregulation of genes associated with adaptive immunity (<italic>mica</italic>, <italic>hla-dpa1</italic>, <italic>hla-dpb1</italic>, and <italic>hla-dqb2</italic>) suggested impaired immune function. Additionally, the composition of the intestinal microbiota was dominated by <italic>Aeromonas</italic>, <italic>Citrobacter</italic>, and <italic>Acinetobacter</italic> in the control group; but there was a significant decrease in the abundance of <italic>Citrobacter</italic> and <italic>Acinetobacter</italic>, and a significantly increased in <italic>Shewanella</italic> and <italic>Hafnia-Obesumbacterium</italic> after acute heat stress. Correlation analyses revealed that changes in the abundance of <italic>Hafnia-Obesumbacterium</italic>, <italic>Buttiauxella</italic>, and <italic>Pseudomonas</italic> were closely associated with changes in gene expression associated with stress, inflammation, and immunity. These results comprehensively demonstrate the adaptive mechanisms of the <italic>G. eckloni</italic> intestine in response to acutely high temperatures and provide a theoretical basis for the future advancement of artificial culture of cold-water fish.</p>