Parental influence on brown trout offspring immune cell composition: An infection study with Tetracapsuloides bryosalmonae

Transgenerational immune priming (TGIP) is a phenomenon by which an initial exposure to a pathogen, here Tetracapsuloides bryosalmonae (causative agent of Proliferative Kidney Disease), stimulates the subsequent immune response to the same or a different pathogen in future generations. The impact of rearing conditions in previous generations, regardless of their exposure to the pathogen, on the immune cell composition and immune response in subsequent generations has not yet been investigated in the brown trout-T. bryosalmonae system. In the present work, we performed flow cytometry to analyze immune cell populations of brown trout. Parental generations (F0) differed in rearing conditions and exposure to the parasite. The study evaluated the baseline frequencies of IgM+ B cells, myeloid cells, and CD8+ T cells in the offspring (F1) young-of-the-year brown trout. Afterwards, F1 fish were experimentally infected with T. bryosalmonae spores and monitored during eight weeks post-infection. The kidney was identified as an immune-cell niche dominated by myeloid cells, which represent approximately two-thirds of the total immune cell population, along with a substantial proportion of IgM+ B cells. CD8+ T cells constitute only a minor fraction within this niche. As measured by flow cytometry, the immune-cell frequencies of offspring were largely unaffected by the parental rearing background (F0) and infection history. Parental history had no influence on the outcome of experimental infection. In T. bryosalmonae exposed animals, parasite concentration increased significantly over time. Moreover, a proportional increase in IgM+ B cells and a proportional decrease in myeloid cells over time was observed. However, the increase in IgM+ B cells was also detected in control animals. In conclusion, this study presents the first analysis of immune cell composition in F1 brown trout derived from parents reared under three distinct environmental conditions with varying parasite exposures. Our flow cytometry results highlight the need for alternative approaches to investigate transgenerational immune priming (TGIP) in brown trout.