An underwater unravelling of the immune landscape

This blog post is provided by Christyn Bailey and Helmut Segner and tells the #StoryBehindThePaper for the paper ‘It’s a hard knock life for some: heterogeneity in infection life-history of salmonids influences parasite disease outcomes‘, which was recently published in the Journal of Animal Ecology. You can also listen to the blog post on Soundcloud.

The role of immunity on a population-level has garnered broad interest due to the ongoing pandemic.  It is really remarkable how much variability there is in how we all manage an encounter with a pathogen in terms of our susceptibility, the symptoms we develop, pathogen burden, immune response, severity, recovery and also in how we might transmit the disease. Moreover, how these individual variations in host phenotypes affect the spread and maintenance of a disease on the population level. From this perspective, to truly understand the ultimate effect of a disease on a population, the impact on the different individuals that make up a population must be assessed.

We decided to take this question underwater and explored the role of host heterogeneity in infection life-history of salmonids and how it influences chronic parasite disease in differential host phenotypes.  We used the myxozoan parasite Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease (PKD) in salmonids as our study system. T. bryosalmonae, the PKD-causing parasite has a two-host life cycle encompassing freshwater bryozoa as invertebrate hosts and mainly salmonid fish as vertebrate hosts. PKD is one of the most serious parasitic diseases of fish and one of several pathogens sensitive to the ongoing climate crisis. It is a well-recognised conservation threat to wild fish and imposes huge economic constraints on the aquaculture industry. In particular, PKD has been identified as a major driver of population declines of brown trout in Switzerland and a key instigator in wild fish mortality events in the USA. While it is known that the disease results in increased mortality of young-of-the-year fish, little is known of how PKD is dispersed or persists in wild populations or how the disease spreads dependant on the share of susceptible or resistant individuals within the population. The percentage of susceptible individuals within the population depends on several factors, including the environment, infection life-history or co-infections, but also the ontogenetic development of the immune system.

Figure 1: Freshwater bryozoa (Fredericella sultana), an invertebrate host of T. bryosalmonae and commonly found in freshwater habitats. (Photo: Christyn Bailey; © Christyn Bailey)

To investigate this question, we established a complex long-term in vivo experiment featuring multiple diverse experimental groups, something that owing to feasibility, appropriate facilities, labour and time is not often accomplished. We examined how host susceptibility and the immune response to T. bryosalmonae infection, and the disease PKD, varied across different infection life-history stages and how it differs between naïve, reinfected and persistently infected hosts. We separated our study into two research scenarios: 1) immune ontogeny and 2) protective immunity. To investigate immune ontogeny, we compared disease progression and outcome in fish with different age classes infected for the first time, this included young-of-the-year fish (YOY – those born this year) fish, and juvenile 1+ fish (those fish born the previous year aged between one and two). To investigate protective immunity, we studied juvenile 1+ fish surviving their first infection as YOY fish. These fish were placed into experimental groups that would either be reexposed or not reexposed and response phenotypes were assigned post-hoc dependant on infection status. In fish not reexposed this included fish that cleared infection (CI) or had a persistent infection (PI). In fish reexposed these included fish that were reinfected (RI), or reexposed and uninfected (RCI) We assessed both parasite centric (infection prevalence, parasite burden, malacospore transmission) and host centric parameters (growth rates, disease severity, infection tolerance and the immune response).

Figure 2: Investigating a typical freshwater habitat in which the parasite could be found (Photo: Maricruz Guevara Soto; © Christyn Bailey)

Our results showed significant variations in the different age phenotypes concerning both parasite infection success and the host response. In younger fish, the parasite proliferated quicker, and disease severity was increased, thus PKD was more intense in these fish. This observation can be validated by the lower infection tolerance and the difference in immune response patterns, which may indicate reduced immunocompetence in younger fish and that may have contributed to the increased immunopathology and disease symptoms observed. Previous PKD research has focused almost exclusively on YOY fish due to supposed increased mortality and indeed, from our results it would appear there is an ontogenetic decline of brown trout in T. bryosalmonae susceptibility.

While concerning protective immunity in the infected fish (PI and RI) parasite burden, disease severity and infection tolerance were comparable. Both PI and RI fish continuously transmitted parasitic fish malacospores and simultaneously maintained an active adaptive immune response throughout our experiment. This might indicate that consistent parasite replication and development occurs in the host as determined by fish malacospore release and stable parasite intensity measurements, and that these processes may provide a continuous source of parasite antigens that stimulates the host immune response and through this process might serve to maintain host immunity. Furthermore, several noteworthy variations were observed in the immune response patterns between the infected treatments, such as the stronger expression in the RI fish of all secretory immunoglobulin transcripts (IgM, IgT, IgD) relative to the PI, CI, RCI treatments. This outcome in RI fish (that an increased antibody type response is exhibited but no increase in disease severity is found) points towards a form of concomitant immunity transpired. Therefore, from the disease outcomes observed in these fish, it appears that the population may contain fish that either avoid infection completely, clear the infection and can avoid reinfection or are persistently infected which may be susceptible to re-infection.

Our findings deliver insight into unravelling the maintenance and spread of a serious parasitic fish disease on an individual and population level, in which only fragmentary knowledge existed. We identified several distinctive features of immune ontogeny and protective mechanisms in this salmonid fish-myxozoan-parasite model not previously investigated. Collectively this highlights two key points that are often overlooked in fish disease modelling a) the importance of the cohort, and b) individual disease susceptibility. We often tend to treat fish like uniform clones but this may not always be the case.

Figure 3: A young-of-the-year brown trout from Switzerland (the vertebrate host of T. bryosalmonae). This fish is at the age class that has been reported to suffer the most from PKD mortalities in a country that has also reported population declines of this species. (Photo: Christian Kropf; © Christyn Bailey)

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