Limited early transcriptome-wide mucosal response to the bacterial pathogen Yersinia ruckeri in Atlantic salmon (Salmo salar) alevins

Abstract

Atlantic salmon larvae possess immune structures, effector cells, and molecules, and their mucosal organs serve as critical barriers against pathogens. But despite these defences, fish larvae show limited immune response capabilities, and the early transcriptomic responses of different mucosal surfaces remain poorly understood. Therefore, this study investigated the transcriptomic landscape of Atlantic salmon (Salmo salar) alevins exposed to the pathogen Yersinia ruckeri, analysing three mucosal organs (skin, gills, and tongue) over 72 h post-exposure. RNA-Seq analysis revealed distinct basal transcriptomic profiles among organs, with gill and tongue showing similarities possibly due to anatomical proximity. Following pathogen exposure, organ-specific immune responses emerged, though relatively subdued in magnitude. The tongue showed peak response at 24 h with 117 differentially expressed genes (DEGs), while skin demonstrated the strongest response at 72 h with 483 DEGs. Notably, 18 shared DEGs between these responses encoded acute-phase proteins, indicating activated mucosal inflammatory responses. The skin exhibited 64 enriched Biological Processes (BP) related to metabolism, gene regulation, and innate immunity at 72 h. In contrast, 33 BP terms enriched in the tongue at 24 h were associated with the regulation of micro- and macromolecules, including lipids, proteins, glucose, and organic acids. Notably, 11 BP terms were common between the two organs, primarily linked to blood coagulation, wound healing, and hemostasis. These findings illuminate host-pathogen interactions at mucosal sites during early development and provide new insights into the temporal dynamics of mucosal immunity to Y. ruckeri in salmon alevins. Furthermore, this study provides the first evidence that the teleost tongue contributes to host immunity.