Transcriptomic signatures differentiating carrier and dead-end fish hosts of proliferative kidney disease

Tetracapsuloides bryosalmonae is the causative agent of proliferative kidney disease (PKD) in salmonids. Brown trout function as a carrier host, while rainbow trout serve as a dead-end host. However, the molecular mechanisms underlying these host-specific differences remain poorly understood. Therefore, in the present study, we aimed to identify host-specific transcriptomic signatures distinguishing carrier and dead- end host.

Comparative transcriptomic analysis of infected kidneys from brown trout and rainbow trout was performed to identify differential gene expression patterns associated with host-specific responses to T. bryosalmonae. Differentially expressed transcripts unique to each host species were identified and subjected to functional enrichment analyses.

A total of 636 and 1,348 unique transcripts were upregulated and downregulated in the infected kidney of brown trout, respectively. In contrast, 526 and 586 unique transcripts were upregulated and downregulated in the infected kidney of rainbow trout, respectively. The uniquely upregulated transcripts in infected brown trout were mainly associated with cell cycle and mitotic cell cycle-related processes, whereas in infected rainbow trout, they were associated with the regulation of biological quality, intracellular signal transduction, and response to chemical stimulus. Similarly, uniquely downregulated transcripts in infected brown trout were mainly associated with anatomical structure morphogenesis, cellular developmental processes, cell differentiation, animal organ development, and cell surface receptor signaling, whereas in infected rainbow trout, they were associated with transmembrane transport, ion transport, and nervous system development.

Our findings suggest that host-specific transcriptomic signatures and their differential regulation underlie the contrasting immune responses of brown trout and rainbow trout against T. bryosalmonae. Such distinct transcriptomic regulation facilitates intra-luminal sporogonic stages of the European strain of T. bryosalmonae in the kidneys of the carrier host, while restricting its development in the dead-end host. Overall, these findings indicate that brown trout maintains a regulated, proliferation-associated environment compatible with parasite development, whereas rainbow trout mounts an immune-dominated response that may restrict parasite sporogenesis. This study provides new insights into the molecular basis of host-specific outcomes in PKD and highlights the role of transcriptional regulation in shaping host-parasite interactions.