RNA-seq analysis reveals the dynamic regulation of proteasomal and autophagic degradation systems of rainbow trout (Oncorhynchus mykiss) skeletal muscle challenged with infectious pancreatic necrosis virus (IPNV)

Abstract

Infectious pancreatic necrosis virus (IPNV) is a critical pathogen causing high salmonid mortality worldwide. IPNV primarily replicates in internal fish organs such as the head kidney, spleen, and pancreas, triggering necrosis and other subclinical symptoms. To date, there are significant data regarding the molecular bases underlying IPNV infection in classic immune tissues (e.g., head kidney and spleen); however, the effects of IPNV in nonclassical immune tissues such skeletal muscle have not been established. In this work, RNA-seq analysis was performed to examine the transcriptional response of rainbow trout skeletal muscle challenged with IPNV. Twenty-eight juvenile rainbow trout were intraperitoneally administered vehicle or IPNV for five and ten days. Total RNA from the skeletal muscle of each fish was obtained and sequenced using NovaSeq Illumina technology. A total of 1,278,349,708 high-quality reads were mapped onto the reference rainbow trout genome enriched with a de novo assembled transcriptome. Transcriptome analysis revealed that 245 and 763 genes were differentially expressed after five and ten days of IPNV challenge, respectively. GO enrichment analyses revealed that the main biological processes modulated in rainbow trout skeletal muscle during IPNV challenge correspond to catabolism-related processes such proteolysis, the ubiquitin-proteasome system, and autophagy. In line with these results, key catabolism-related signaling pathways, such as proteasome and FoxO signaling, were greatly impacted in our in vivo assay. Interestingly, most of these catabolism-related processes and signaling pathways in skeletal muscle were first downregulated after five days of IPNV administration and then were upregulated after ten days. Considering the results obtained in this work, we propose that IPNV is involved in the physiological response of skeletal muscle in salmonids by modulating critical catabolism-related processes.