Who needs the hotspot? The effect of temperature on the fish host immune response to Tetracapsuloides bryosalmonae the causative agent of proliferative kidney disease

Abstract

Proliferative kidney disease (PKD) of salmonids, caused by Tetracapsuloides bryosalmonae may lead to high mortalities at elevated water temperatures. However, it has not yet been investigated how temperature affects the fish host immune response to T. bryosalmonae. We exposed YOY (young of the year) rainbow trout (Oncorhynchus mykiss) to T. bryosalmonae at two temperatures (12 °C and 15 °C) that reflect a realistic environmental scenario and could occur in the natural habitat of salmonids. We followed the development of the parasite, host pathology and immune response over seven weeks. We evaluated the composition and kinetics of the leukocytes and their major subgroups in the anterior and posterior kidney. We measured immune gene expression profiles associated with cell lineages and functional pathways in the anterior and posterior kidney. At 12 °C, both infection prevalence and pathogen load were markedly lower. While the immune response was characterized by subtle changes, mainly an increased amount of lymphocytes present in the kidney, elevated expression of Th1-like signature cytokines and strong upregulation of the natural killer cell enhancement factor, NKEF at week 6 P.E. At 15 °C the infection prevalence and pathogen burden were ominously greater. While the immune response as the disease progressed was associated with a Th2-like switch at week 6 P.E and a prominent B cell response, evidenced at the tissue, cell and transcript level. Our results highlight how a subtle, environmentally relevant difference in temperature resulted in diverse outcomes in terms of the immune response strategy, altering the type of interaction between a host and a parasite.

Are brown trout Salmo trutta fario and rainbow trout Oncorhynchus mykiss two of a kind? A comparative study of salmonids to temperature‐influenced Tetracapsuloides bryosalmonae infection

“…In these studies, parasite intensity was significantly greater in kidneys of brown trout compared with rainbow trout, similar to the present study (Kumar et al, 2013), whereas only rainbow trout showed severe clinical signs of PKD in contrast to brown trout (Grabner & El-Matbouli, 2008). Reports have separately explored how temperature influences the development of T. bryosalmonae in either brown trout (Wahli, Bernet, Segner, & Schmidt-Posthaus, 2008) or rainbow trout (Bailey et al, 2017;), but they have not yet investigated the influence of temperature from the confirmation of infection onwards with a defined dose identical for both species, in these species, in a comparative fashion.…”

“…In these studies, parasite intensity was significantly greater in kidneys of brown trout compared with rainbow trout, similar to the present study (Kumar et al., ), whereas only rainbow trout showed severe clinical signs of PKD in contrast to brown trout (Grabner & El‐Matbouli, ). Reports have separately explored how temperature influences the development of T. bryosalmonae in either brown trout (Wahli, Bernet, Segner, & Schmidt‐Posthaus, ) or rainbow trout (Bailey et al., ; Bettge, Wahli, Segner, & Schmidt‐Posthaus, ; Bettge, Segner et al., ), but they have not yet investigated the influence of temperature from the confirmation of infection onwards with a defined dose identical for both species, in these species, in a comparative fashion. By focusing on parasite kinetics, influence of temperature on the processes and differences between the two fish species, we provide a different perspective to earlier studies which focused on the development of clinical PKD (Bettge, Segner et al., ; Bettge, Wahli et al., ; Grabner & El‐Matbouli, ; Kumar et al., ).…”

“…Climate change may act directly on host–pathogen systems via processes altering the pathogen virulence and transmission, as well as host susceptibility or indirectly via ecological mechanisms (Bailey, Segner, Casanova‐Nakayama, & Wahli, ; Gallana, Ryser‐Degiorgis, Wahli, & Segner, ). Pertinent to this is PKD of salmonids in which increasing water temperatures in connection with global warming have been linked with increased mortalities of wild brown trout (Burkhardt‐Holm et al., ; Wahli et al., , ) and farmed rainbow trout populations (Okamura, Schmidt‐Posthaus, & Wahli, ).…”

Trade-Offs Underwater: Physiological Plasticity of Rainbow Trout (Oncorhynchus mykiss) Confronted by Multiple Stressors

“…The immune system response under the various treatments was assessed by measuring the organ somatic indices of two key immune organs in fish-the head kidney (HKSI) and spleen (SSI)-as well as the mRNA transcript levels of immune genes involved in the host response of rainbow trout to the infection by T. bryosalmonae. The selection of the genes was based on the findings reported by Bailey et al [51] and Gorgoglione et al [57] on the rainbow trout immune response to T. bryosalmonae infection.…”

“…Infection intensity of the fish by the parasite reaches maximum values towards autumn, when the fish physiologically prepares for winter. Under the experimental conditions chosen in the present study, the parasite causes a long-term infection and corresponding immune response without causing gross mortalities [51,52]. All three chosen environmental stressors are real world stressors that co-occur in the aquatic habitats of salmonids.…”