Proliferative kidney disease is an emerging infectious disease of salmonids modulated by climate change, state Christyn Bailey and Thomas Wahli from the University of Bern’s Centre for Fish and Wildlife Health.
Global climate change has major effects on the environment, whereby aquatic habitats are increasingly affected, be it by alterations of water flow or by increased temperatures. The latter is a particularly important factor, as many animals living in the aquatic milieu are poikilothermic and thus react much more to changes in temperature than homoiothermic terrestrial animals.
A prime example of such an effect is the decrease of brown trout populations in Switzerland. Here, on one hand a direct effect of increased water temperature is suspected as one possible reason, as the upper thermal range of the suitable temperature for this species is often surpassed. However, as a further potential actor for this decrease, an indirect effect by an infectious disease is suspected to play a pivotal role.
Proliferative kidney disease and tetracapsuloides bryosalmonae
This disease, proliferative kidney disease is caused by the myxozoan parasite Tetracapsuloides bryosalmonae. Myxozoans are multicellular organisms considered to be stripped down relatives to the jelly fish (cnidarians).
T. bryosalmonae mainly affects the kidney of susceptible fish (see Fig. 1) inducing kidney failure characterised by anemia and problems with excretion. The causative agent has a multihost life cycle with bryozoans (minute sessile colony forming animals) as invertebrate hosts and salmonid fish as vertebrate hosts. The disease has shown to be temperature dependent, with the main effect being increased mortalities in fish hosts at elevated temperatures. The question is why elevated water temperature leads to a more severe disease outcome.
Our earlier research demonstrated that parasite dynamics in the fish host are accelerated with increasing water temperature. In fact, we could show that parasite infection success is increased at a warmer temperature, the proliferation rate of the parasite in the fish is faster, and the onset of parasite shedding from the fish host occurs earlier. Together, these processes will promote the infection cycle and disease spread, but they do not yet explain why mortality of the fish host increases, as in particular the maximum load of parasites in the fish host is not affected by temperature.
To gain more insight into the possible causes of the increasing mortality of proliferative kidney disease infected fish occurring at increased water temperatures, we focused on exploring the impact of temperature on the immunocompetence of the fish to manage the infection.
The novelty of our approach was that fish were infected with a defined number of parasite spores over a defined infection window. By this, the immune response was driven only by temperature and parasite development and not confounded by continuous new infections. The course of the disease was then followed until parasite numbers in the fish plateaued.
Under controlled laboratory conditions, we compared the fish immune response to the parasite at two temperatures: 12°C (which is well in the optimum physiological range of salmonids), and 15°C (which is closer to the margins of the optimal range).
The temperature difference of 3°C reflects a realistic environmental change as it actually occurs in the natural habitat of salmonids. While many freshwater fish habitats in Switzerland were summer-cold, with water temperatures rarely surpassing 12-14°C, nowadays they often reach temperatures up to 20°C during the summer period. Our immunological studies showed that trout infected with T. byosalmonae at 12°C mounted a rather limited immune response during parasite infection. In contrast, at 15°C the immune response was much more pronounced.
Importantly, there was not only a change in the intensity of the immune response but also in the type of immune response (see Fig. 2). At 15°C there was a clear shift to a humoral immune response – this was evident from a dysregulation of B cell subsets.
Overall, at 12°C the fish during infection appears to have increased tolerance towards the parasite and limited the harm caused by the parasite – a response being suggestive for a coevolved host-parasite system. In contrast, at 15°C, the fish seems to increase resistance traits to attempt to eliminate the parasite, with higher intensity of the immune response and ensuing immunopathology. Thus, the devastating effect of increasing temperature on the disease appears to go along with a temperature-driven change in the immune response of the fish host.
Protecting against re-infection
Surviving a first proliferative kidney disease infection is critical for the fish host, as this can result in at least partial protection to re-infection. This has been shown in an experiment using one-year old rainbow trout. In this experiment, a group of fish had been exposed to T. bryosalmonae in their first year of life, whereas a second group of fish of the same origin was not exposed but kept under the same conditions as the exposed ones.
In the second year of life of both groups (i.e. those previously infected and those not previously infected) the fish were exposed to an identical number of parasites. While the previously un-exposed animals developed clear signs of proliferative kidney disease with high parasite burdens, kidney swelling and a prevalence of 100%, re-exposed animals showed lower parasite burdens, less alterations and lower infection prevalence.
The finding that survivors from the first year are protected from severe disease symptoms in the second and probably subsequent years of life has important implications for the impact of the disease on the fish populations as it indicates that the disease will interfere with population growth and recruitment mainly, if not exclusively, via elevated mortalities of the early life stage of salmonids.
Expanding the experimental scope
All these experiments had been performed with rainbow trout, a fish species introduced to Europe from North America for farming purposes. Therefore, the next step, was to determine whether the brown trout a native species to Europe reacts in the same way to an infection by T. bryosalmonae as rainbow trout. To answer this question, infection prevalence and the time course of the infection was compared in fish of both species exposed to identical parasite loads under identical conditions but at two different temperatures i.e. 12°C and 15°C. The key finding from this study was that brown trout showed the greater sensitivity to the infection than rainbow trout, irrespective of the temperature.
The different outcome in the two closely-related salmonid species indicates that the same environmental change can result in different consequences. Additionally, we investigated if the two-salmonid species, rainbow trout and brown trout, differ in their immune response
to T. bryosalmonae.
At a temperature of 15°C, the immune response of brown trout, comparable to rainbow trout, was also characterised by a B cell response. Nevertheless, there also existed differences between the two species, the clearest difference being a sequential one.
Expression of immune relevant genes in rainbow trout started much earlier (from 14 days post exposure onwards) than in brown trout (from 30-40 d.p.e.). Interestingly, these species-specific differences in the immune response correlate with a species difference in the capacity to clear the parasite from the host: while rainbow trout can fully clear the parasite load after infection, complete parasite clearance has not yet been demonstrated in brown trout.
Lessons to be learned
• A moderate change in environmental temperature can strongly increase the severity of the parasite-induced proliferative kidney disease for salmonids, making this disease an emerging one
• The temperature effect on PKD severity is driven, at least in part, by a temperature effect on the fish immune response towards the parasite infection
• Salmonid species react differently to the parasite infection and show different sensitivity to the temperature influence
Centre for Fish and Wildlife Health
Department of Infectious Diseases and Pathobiology
University of Bern