Integrated Analysis of mRNA-Seq and MiRNA-Seq Reveals the Molecular Mechanism of the Intestinal Immune Response in Marsupenaeus japonicus Under Decapod Iridescent Virus 1 Infection

Abstract

The intestine is not only an important digestive organ but also an important immune organ for shrimp; it plays a key role in maintaining homeostasis. Decapod iridescent virus 1 (DIV1) is a new type of shrimp-lethal virus that has received extensive attention in recent years. To date, most studies of the shrimp intestinal immune response under viral infections have relied on single omics analyses; there is a lack of systematic multi-omics research. In the current study, intestinal mRNA-seq and microRNA (miRNA)-seq analyses of Marsupenaeus japonicus under DIV1 infection were performed. A total of 1,976 differentially expressed genes (DEGs) and 32 differentially expressed miRNAs (DEMs) were identified. Among them, 21 DEMs were negatively correlated with 194 DEGs from a total of 223 correlations. Functional annotation analysis revealed that M. japonicus can regulate glycosaminoglycan biosynthesis (chondroitin sulfate, dermatan sulfate, and keratan sulfate), vitamin metabolism (retinol metabolism and ascorbate and aldarate metabolism), immune pathway activation (Toll and IMD signaling pathways, Wnt signaling pathway, IL-17 signaling pathway, and Hippo signaling pathway), immunity enzyme activity promotion (triose-phosphate isomerase), antimicrobial peptide (AMP) expression, reactive oxygen species (ROS) production, and cell apoptosis through miRNAs to participate in the host’s antiviral immune response, while DIV1 can influence Warburg effect-related pathways (pyruvate metabolism, glycolysis/gluconeogenesis, and citrate cycle), glycosphingolipid biosynthesis-related pathways (glycosphingolipid biosynthesis—globo and isoglobo series and glycosphingolipid biosynthesis—lacto and neolacto series), and the tight junction and adhesion junction of the intestinal mucosal epithelium through the host’s miRNAs and mRNA to promote its own invasion and replication. These results indicate that intestinal miRNAs play important roles in the shrimp immune response against DIV1 infection. This study provides a basis for further study of the shrimp intestinal antiviral immune response and for the formulation of effective new strategies for the prevention and treatment of DIV1 infection.

Integrated analysis of intestinal microbiota and metabolomic reveals that decapod iridescent virus 1 (DIV1) infection induces secondary bacterial infection and metabolic reprogramming in Marsupenaeus japonicus

“…In addition, some amino acid metabolism-related pathways were also significantly enriched under DIV1 infection, including “tyrosine metabolism”, “phenylalanine metabolism” and “alanine, aspartate and glutamate metabolism”. These phenomena also appeared in previous studies (Liao et al, 2020; He et al, 2021b; He et al, 2022), which may be attributed to the material and energy requirements of DIV1 replication and suggested that DIV1 may contain AMGs for regulating host amino acid metabolism, carbohydrate metabolism and energy metabolism. It was worth noting that some pathways related to vitamin metabolism were significantly enriched, such as “retinol metabolism”, “vitamin B6 metabolism” and “pantothenate and CoA biosynthesis”.…”

“…To date, several crustacean viruses have been found to induce metabolic reprogramming to promote survival and replication, including white spot syndrome virus (WSSV) (Chen et al, 2011; Hsieh et al, 2015; Apún-Molina et al, 2017; Godoy-Lugo et al, 2019), Taura syndrome virus (TSV) (Zeng et al, 2014) and IHHNV (Galvan-Alvarez et al, 2012). In recent years, with global warming and increasing marine pollution, some novel marine viruses have become widespread in the aquaculture industry, causing huge losses to the aquaculture industry (He et al, 2022). Decapod iridescent virus 1 (DIV1) is one of the newly discovered marine viruses.…”

“…Due to its high economic value, strong environmental adaptability and suitability for long-distance transportation, it has now become one of the most farmed prawns in China (He et al, 2020; Yuan et al, 2016). Our previous study demonstrated that M. japonicus was a susceptible host to DIV1 (He et al, 2021a; He et al, 2022). Through mRNA-seq and miRNA-seq analyses and their association analysis, we preliminarily revealed the hemocyte and intestinal immune response of M. japonicus to DIV1 infection (He et al, 2021a; He et al, 2022), and proposed that DIV1 can promote the Warburg effect by regulating host miRNA and mRNA expression.…”

“…Our previous study demonstrated that M. japonicus was a susceptible host to DIV1 (He et al, 2021a; He et al, 2022). Through mRNA-seq and miRNA-seq analyses and their association analysis, we preliminarily revealed the hemocyte and intestinal immune response of M. japonicus to DIV1 infection (He et al, 2021a; He et al, 2022), and proposed that DIV1 can promote the Warburg effect by regulating host miRNA and mRNA expression. The Warburg effect was also observed in DIV1-infected Litopenaeus vannamei and Penaeus monodon .…”

Integrated Analysis of miRNA-mRNA Expression in Mink Lung Epithelial Cells Infected With Canine Distemper Virus

“…In recent years, high-throughput sequencing techniques were used to determine the expression profiles of miRNAs in animals, plants and viruses. Some studies showed that the integrated analysis of miRNA and mRNA in viral infection samples could confirm the regulatory mechanism of miRNA ( 28 – 30 ). The analysis of giant pandas in captivity vaccinated against CDV was operated with miRNA-mRNA.…”