Blood Transcriptomics of Turbot Scophthalmus maximus: A Tool for Health Monitoring and Disease Studies

SIMPLE SUMMARY: The analysis of blood gene expression is emerging as a relevant source of information about the health status of an organism. While these investigations are increasingly performed in human and terrestrial animals, their potential is still underexplored in fish pathology. The aim of this work was to analyze the blood transcriptional profile of a commercially important flatfish species, turbot (Scophthalmus maximus), in healthy and diseased specimens. The analysis of the most expressed genes in healthy fish indicated that turbot red blood cells have important immunological functions. In diseased fish, parasitized by a myxozoan, the blood analysis reflected a broad inhibition of the immune response followed by intense inflammatory activation in heavy infections. The results showed that turbot response appears delayed, dysregulated and ineffective in stopping the infection. Particularly, a proper development of the adaptive immune response was lacking. This study points out that blood gene expression profiling is a reliable tool for health monitoring, as well as to advance in the knowledge of fish immunity and diseases. ABSTRACT: Blood transcriptomics is emerging as a relevant tool to monitor the status of the immune system and assist in diagnosis, prognosis, treatment and pathogenesis studies of diseases. In fish pathology, the potential of transcriptome profiling of blood is still poorly explored. Here, RNA sequencing was applied to analyze the blood transcriptional profile of turbot (Scophthalmus maximus), the most important farmed flatfish. The study was conducted in healthy specimens and specimens parasitized by the myxozoan Enteromyxum scophthalmi, which causes one of the most devastating diseases in turbot aquaculture. The blood of healthy turbot showed a transcriptomic profile mainly related to erythrocyte gas transportation function, but also to antigen processing and presentation. In moderately infected turbot, the blood reflected a broad inhibition of the immune response. Particularly, down-regulation of the B cell receptor signaling pathway was shared with heavily parasitized fish, which showed larger transcriptomic changes, including the activation of the inflammatory response. Turbot response to enteromyxosis proved to be delayed, dysregulated and ineffective in stopping the infection. The study evinces that blood transcriptomics can contribute to a better understanding of the teleost immune system and serve as a reliable tool to investigate the physiopathological status of fish.