In the Shadow: The Emerging Role of Long Non-Coding RNAs in the Immune Response of Atlantic Salmon

The genomic era has increased the research effort to uncover how the genome of an organism, and specifically the transcriptome, is modulated after interplaying with pathogenic microorganisms and ectoparasites. Here, common and exclusives molecular signaling pathways have been disentangled, making significant contributions to cope infection diseases that impact the global aquaculture. However, the ever-increasing accessibility of sequencing technology has also evidenced functional roles of long non-coding RNAs (lncRNAs) related to several biological processes including immune response. The discovery of lncRNAs gives the opportunity to investigate the transcriptome dismissed as junk DNA and involved in fish immunity. This study reports a comprehensive transcriptome analysis of lncRNAs from Atlantic salmon (Salmo salar) infected with the most prevalent pathogens in the Chilean salmon aquaculture: the infectious salmon anemia virus (ISAv), the intracellular bacteria Piscirickettsia salmonis and the ectoparasite copepod Caligus rogercresseyi. Challenge trials were independently carried out according to protocols established for each pathogen, where head-kidney, gills, liver, brain, skin and spleen tissues were sampled and subsequently used for RNA purification. Directional cDNA libraries were constructed for Illumina sequencing, which profiled polyadenylated, coding, and noncoding transcripts, but not small RNAs. De novo assembly, lncRNAs discovery and differentially expressed transcripts were analyzed using CLC Genomics Workbench software and additional bioinformatics tools. The following findings were evidenced: (i) Most lncRNAs were regulated in response to ISAv, P. salmonis and C. rogercresseyi infection; (ii) The transcript subsets were uniquely modulated in each tissue evaluated; and (iii) A subset of lncRNAs was upregulated for each tissue and time analyzed, indicating potential markers for pathogen infection. These findings represent the first discovery for the widespread differential expression of lncRNAs in response to virus, bacteria and ectoparasite infections in no-model species, suggesting that lncRNAs could be involved in regulating the fish immune response.