The Atlantic salmon tongue mucosa functions as an active mucosal immune site capable of responding to a pathogen

The tongue of teleost fish is a mucosal organ whose role in immunity remains largely understudied. Here, we performed transcriptomic analyses of the Atlantic salmon (Salmo salar) smolt tongue to investigate its baseline gene expression profile and its immune response to a bacterial challenge with Yersinia ruckeri. In the unstimulated state, transcriptomic profiling revealed that the tongue is a highly metabolically active organ with enrichment of genes involved in cytoskeletal organisation, transport, and metabolism. Gene ontology (GO) analysis identified terms associated with immune system processes indicating that the tongue maintains a state of immune readiness even in the absence of infection or pathogenic stimulation. The transcriptional body map further revealed that the tongue shares gene expression features at the naïve state with both muscular and mucosal tissues including genes related to immunity. Following bacterial exposure both ex vivo and in vivo, an immune response was observed and was characterised by the upregulation of cytokines, chemokines, and antimicrobial effectors. GO and KEGG pathway enrichment analyses identified activation of immune- and metabolism-related pathways, including immune signalling, oxidative phosphorylation, lysosome, and phagosome pathways, thus reflecting the high energetic demand of the immune response to the bacterial pathogen. These findings collectively reveal that a transient bacterial challenge elicits a metabolically demanding immune response in the salmon tongue driven by coordinated regulation of immune signalling and cellular metabolic pathways. This study demonstrates that the Atlantic salmon tongue is an active component of the mucosal immune system and provides novel insights into the intersection of metabolism and immunity in fish mucosal organs, particularly in response to a transient bacterial challenge.