Investigation of Gene Networks in Three Components of Immune System Provides Novel Insights into Immune Response Mechanisms against Edwardsiella tarda Infection in Paralichthys olivaceus

SIMPLE SUMMARY: Paralichthys olivaceus, a common marine fish, is susceptible to various harmful organisms. One such organism, Edwardsiella tarda, is a particularly potent pathogen that can cause severe illness and even death in fish during prolonged infections. The gills, blood, and kidneys, which are crucial components of the immune system in these fish, play vital roles in immune responses, including in the differentiation of immune cells, removal of diseased cells, and other immunity-related processes. In this study, we infected Paralichthys olivaceus with Edwardsiella tarda and analyzed the genetic information of three components at different timepoints after infection. By using advanced analytical techniques, we identified specific genes and gene networks associated with the immune response. Our innovative approach allowed us to gain a deeper understanding of how the immune system of Paralichthys olivaceus responds to Edwardsiella tarda infection in these important components. These findings provide valuable genetic resources for studying immunity in Paralichthys olivaceus and contribute to our knowledge of the molecular mechanisms underlying Edwardsiella tarda infections in fish. ABSTRACT: As a quintessential marine teleost, Paralichthys olivaceus demonstrates vulnerability to a range of pathogens. Long-term infection with Edwardsiella tarda significantly inhibits fish growth and even induces death. Gills, blood, and kidneys, pivotal components of the immune system in teleosts, elicit vital regulatory roles in immune response processes including immune cell differentiation, diseased cell clearance, and other immunity-related mechanisms. This study entailed infecting P. olivaceus with E. tarda for 48 h and examining transcriptome data from the three components at 0, 8, and 48 h post-infection employing weighted gene co-expression network analysis (WGCNA) and protein–protein interaction (PPI) network analysis. Network analyses revealed a series of immune response processes after infection and identified multiple key modules and key, core, and hub genes including xpo1, src, tlr13, stat1, and mefv. By innovatively amalgamating WGCNA and PPI network methodologies, our investigation facilitated an in-depth examination of immune response mechanisms within three significant P. olivaceus components post-E. tarda infection. Our results provided valuable genetic resources for understanding immunity in P. olivaceus immune-related components and assisted us in further exploring the molecular mechanisms of E. tarda infection in teleosts.