Comparative multi-transcriptomic analysis of Atlantic salmon (Salmo salar) under distinct pathogen infections

Abstract

Atlantic salmon is among the most widely farmed species globally. The large-scale cultivation of salmon inevitably results in the emergence of diverse diseases, highlighting the critical need to investigate host-pathogen interaction. While numerous transcriptomic analyses have been reported for infected Atlantic salmon, there is a notable lack of comprehensive studies directly comparing transcriptomic responses across different pathogens. Furthermore, differences in bioinformatic methodologies among individual studies present challenges for integrating immunological characteristics in response to various pathogen types. In this research, we performed a comparative multi-transcriptomic analysis utilizing 82 publicly available head kidney transcriptomes from Atlantic salmon that were independently infected with Piscirickettsia salmonis, infectious salmon anemia virus (ISAV), pilchard orthomyxovirus (POMV), or exposed to amoebic gill disease (AGD) in separate experimental settings. Despite inherent batch effects, transcriptome signatures were consistently correlated with specific pathogen types. In particular, infections with major pathogens (P. salmonis, POMV, ISAV, and AGD) triggered distinct pathogen-specific transcriptomic responses. P. salmonis was characterized by the unique activation of actin cytoskeleton remodeling and associated cell signaling pathways. Although POMV and ISAV are classified within the same viral family, their activated biological pathways demonstrated considerable disparity. For instance, POMV infection led to activation of proteasome activity and protein processing in endoplasmic reticulum pathways, whereas ISAV infection predominantly downregulated numerous biological processes. AGD infection was marked by a pronounced upregulation of metabolic-related pathways relative to overall immune responses. This indicates that AGD infection substantially influences the host's metabolic pathways, potentially affecting health status and disease susceptibility. The comparative multi-transcriptomic analysis conducted here thus advances our understanding of immunological responses and host-pathogen interactions in Atlantic salmon by elucidating unique patterns of transcriptomic expression.