The effect of acute heat stress on the innate immune function of rainbow trout based on the transcriptome

Zhou, Changqing; Ka, Wei; Yuan, Weike; Wang, Jianlin

doi:10.1016/j.jtherbio.2021.102834

Cited by 27 publications

(13 citation statements)

References 53 publications

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“…According to our previous study ( Zhou et al, 2019 , 2021 ), the water temperature was rapidly increased from 16 to 22.5°C within 2 h, then this temperature was maintained (22.5°C) for 48 h, which led to ∼ 50% death of rainbow trouts ( n = 90). Therefore, we speculated that 22.5°C may be a threshold for rainbow trout to cope with acute heat stress.…”

Section: Methodsmentioning

confidence: 92%

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Association of Gut Microbiota With Metabolism in Rainbow Trout Under Acute Heat Stress

Zhou

Yang²,

Ka³

et al. 2022

Front. Microbiol.

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Global warming is one of the most common environmental challenges faced by cold-water fish farming. Heat stress seriously affects the feeding, growth, immunity, and disease resistance of fish. These changes are closely related to the destruction of intestinal barrier function, the change of intestinal microbiota, and metabolic dysfunction. However, the causal relationship between the phenotypic effects of heat stress as well as intestinal and metabolic functions of fish is unknown. In the current study, the optimal growth temperature (16°C) of rainbow trout was used as the control group, while the fish treated at 22.5°C, 23.5°C, and 24.5°C for 24 h, respectively, were the treatment groups. The 16S rRNA gene sequencing analysis showed that with the increase in temperature, the relative abundance and diversity of intestinal microbiota decreased significantly, while the number of Mycoplasma, Firmicutes, and Tenericutes increased significantly. Non-targeted metabolomics analysis by liquid chromatography-mass spectrometry analysis and correlation analysis showed that the changes of metabolites related to amino acids, vitamins, and short-chain fatty acids in serum of rainbow trout under acute heat stress were strongly correlated with the decrease of relative abundance of various intestinal microbiota, especially Morganella, Enterobacter, Lactobacillus, Lawsonia, and Cloacibacterium. In addition, we also found that acute heat stress seriously affected the intestinal structure and barrier function, and also caused the pathological damage of epithelial cells. These results indicate that the gut microbiome of acute heat-stressed rainbow trout could mediate metabolite transfer through the gut barrier by affecting its integrity. Significant changes in gut morphology, permeability, antioxidant capacity, and pro-inflammatory cytokine levels were observed. Therefore, it is necessary to explore the changes of intestinal microbiota under heat stress to help understand the regulatory mechanism of heat stress and protect the intestinal health of rainbow trout from the negative effects of rising water temperature.

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Section: Methodsmentioning

confidence: 92%

“…Stress refers to a series of systemic reactions caused by the destruction or interference of body homeostasis ( Wendelaar, 1997 ; Zhou et al, 2019 , 2021 ). With global climate change, heat stress has become a threat to fish farming.…”

Section: Introductionmentioning

confidence: 99%

Association of Gut Microbiota With Metabolism in Rainbow Trout Under Acute Heat Stress

Zhou

Yang²,

Ka³

et al. 2022

Front. Microbiol.

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“…The sequencing of lncRNAs was completed by the Illumina HiSeq platform (Wuhan, China). The construction of cDNA libraries and high-throughput sequencing work refers to our previously published research [10]. Clean reads were obtained by filtering raw data, including the removal of rRNA, low-quality reads, contaminated joints, and reads with high N content in unknown bases were then compared to the reference genome of rainbow trout for transcription assembly.…”

Section: Transcriptome Sequencing and Analysismentioning

confidence: 99%

RNA-Seq Analysis of the Key Long Noncoding RNAs and mRNAs Related to the Regulation of Acute Heat Stress in Rainbow Trout

Zhou

Ka²,

Zhang

et al. 2022

Animals

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As the global climate warms, more creatures are threatened by high temperatures, especially cold-water fish such as rainbow trout. Evidence has demonstrated that long noncoding RNAs (lncRNAs) play a pivotal role in regulating heat stress in animals, but we have little understanding of this regulatory mechanism. The present study aimed to identify potential key lncRNAs involved in regulating acute heat stress in rainbow trout. lncRNA and mRNA expression profiles of rainbow trout head kidney were analyzed via high-throughput RNA sequencing, which exhibited that 1256 lncRNAs (802 up-regulation, 454 down-regulation) and 604 mRNAs (353 up-regulation, 251 down-regulation) were differentially expressed. These differentially expressed genes were confirmed to be primarily associated with immune regulation, apoptosis, and metabolic process signaling pathways through Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway enrichment analysis and coding-noncoding co-expression network analysis. These results suggested that 18 key lncRNA-mRNA pairs are essential in regulating acute heat stress in rainbow trout. Overall, these analyses showed the effects of heat stress on various physiological functions in rainbow trout at the transcriptome level, providing a theoretical basis for improving the production and breeding of rainbow trout and the selection of new heat-resistant varieties.

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“…More recently, RNA-sequencing (RNA-seq) has emerged as a popular method allowing for the entire transcriptome to be assessed rather than a predefined number of transcripts (a potential limiting factor with microarrays). Several studies have examined the impact of elevated temperature on various tissue/organ transcriptomes in multiple fish species using RNA-seq (e.g., Tomalty et al, 2015 ; Tan et al, 2016 ; Veilleux et al, 2018 ; Shi et al, 2019 ; Bowen et al, 2020 ; Pan et al, 2021 ; Quan et al, 2021 ; Yang et al, 2021 ; Zhou et al, 2021 ). However, most of these studies measured responses following acute exposure (i.e., hours to days) to thermal extremes and there is limited information on transcriptomic signatures of fish reared long-term (i.e., months) within typical thermal ranges observed in aquaculture.…”

Section: Introductionmentioning

confidence: 99%

RNA-Seq Analysis of the Growth Hormone Transgenic Female Triploid Atlantic Salmon (Salmo salar) Hepatic Transcriptome Reveals Broad Temperature-Mediated Effects on Metabolism and Other Biological Processes

Ignatz

Hori²,

Kumar

et al. 2022

Front. Genet.

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This study examined the impact of rearing temperature (10.5, 13.5 or 16.5°C) on the hepatic transcriptome of AquAdvantage Salmon (growth hormone transgenic female triploid Atlantic salmon) at an average weight of 800 g. Six stranded PE libraries were Illumina-sequenced from each temperature group, resulting in an average of over 100 M raw reads per individual fish. RNA-sequencing (RNA-seq) results showed the greatest difference in the number of differentially expressed transcripts (1750 DETs), as revealed by both DESeq2 and edgeR (q < 0.05; fold-change > |1.5|), was between the 10.5 and 16.5°C temperature groups. In contrast, 172 and 52 DETs were found in the 10.5 vs. 13.5°C and the 13.5 vs. 16.5°C comparisons, respectively. Considering the DETs between the 10.5 and 16.5°C groups, 282 enriched gene ontology (GO) terms were identified (q < 0.05), including “response to stress”, “immune system process”, “lipid metabolic process”, “oxidation-reduction process”, and “cholesterol metabolic process”, suggesting elevated temperature elicited broad effects on multiple biological systems. Pathway analysis using ClueGO showed additional impacts on amino acid and lipid metabolism. There was a significant positive correlation between RNA-seq and real-time quantitative polymerase chain reaction (RT-qPCR) results for 8 of 9 metabolic-related transcripts tested. RT-qPCR results also correlated to changes in fillet tissue composition previously reported in these salmon (e.g., methionine and lysine concentrations positively correlated with hsp90ab1 transcript expression), suggesting that rearing temperature played a significant role in mediating metabolic/biosynthetic pathways of AquAdvantage Salmon. Many transcripts related to lipid/fatty acid metabolism (e.g., elovl2, fabpi, hacd2, mgll, s27a2, thrsp) were downregulated at 16.5°C compared to both other temperature groups. Additionally, enrichment of stress-, apoptosis- and catabolism-relevant GO terms at 16.5°C suggests that this temperature may not be ideal for commercial production when using freshwater recirculating aquaculture systems (RAS). This study relates phenotypic responses to transcript-specific findings and therefore aids in the determination of an optimal rearing temperature for AquAdvantage Salmon. With approval to grow and sell AquAdvantage Salmon in the United States and Canada, the novel insights provided by this research can help industry expansion by promoting optimal physiological performance and health.

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The effect of acute heat stress on the innate immune function of rainbow trout based on the transcriptome

Cited by 27 publications

References 53 publications

Association of Gut Microbiota With Metabolism in Rainbow Trout Under Acute Heat Stress

Association of Gut Microbiota With Metabolism in Rainbow Trout Under Acute Heat Stress

RNA-Seq Analysis of the Key Long Noncoding RNAs and mRNAs Related to the Regulation of Acute Heat Stress in Rainbow Trout

RNA-Seq Analysis of the Growth Hormone Transgenic Female Triploid Atlantic Salmon (Salmo salar) Hepatic Transcriptome Reveals Broad Temperature-Mediated Effects on Metabolism and Other Biological Processes

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