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

Bailey, Christyn; Schmidt‐Posthaus, Heike; Segner, Helmut; Wahli, Thomas; Strepparava, Nicole

doi:10.1111/jfd.12694

Cited by 16 publications

(19 citation statements)

References 36 publications

(66 reference statements)

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“…Similarly, inhibition of il-1β has been previously reported in the kidney of brown trout infected with Tetracapsuloides bryosalmonae , the agent of proliferative kidney disease (PKD) [78], in the intestine infected with E. leei [79] or C. shasta , the agent of enteronecrosis or gut-rot disease in salmonids [32]. Low expression of ifnγ was previously reported in the kidney during the early stages of PKD (slightly increased by 50 dpi; [80]), while other myxozoan models suggest its increase and possible contribution to the cytotoxic activities [81, 82]. The timing of the downregulation of these genes is in accordance with the increasing expression of il-10 [83].…”

Section: Discussionmentioning

confidence: 99%

The kinetics of cellular and humoral immune responses of common carp to presporogonic development of the myxozoan Sphaerospora molnari

et al. 2019

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Background Sphaerospora molnari is a myxozoan parasite causing skin and gill sphaerosporosis in common carp ( Cyprinus carpio ) in central Europe. For most myxozoans, little is known about the early development and the expansion of the infection in the fish host, prior to spore formation. A major reason for this lack of information is the absence of laboratory model organisms, whose life-cycle stages are available throughout the year. Results We have established a laboratory infection model for early proliferative stages of myxozoans, based on separation and intraperitoneal injection of motile and dividing S. molnari stages isolated from the blood of carp. In the present study we characterize the kinetics of the presporogonic development of S. molnari , while analyzing cellular host responses, cytokine and systemic immunoglobulin expression, over a 63-day period. Our study shows activation of innate immune responses followed by B cell-mediated immune responses. We observed rapid parasite efflux from the peritoneal cavity (< 40 hours), an initial covert infection period with a moderate proinflammatory response for about 1–2 weeks, followed by a period of parasite multiplication in the blood which peaked at 28 days post-infection (dpi) and was associated with a massive lymphocyte response. Our data further revealed a switch to a massive anti-inflammatory response (up to 1456-fold expression of il-10 ), a strong increase in the expression of IgM transcripts and increased number of IgM + B lymphocytes, which produce specific antibodies for the elimination of most of the parasites from the fish at 35 dpi. However, despite the presence of these antibodies, S. molnari invades the liver 42 dpi, where an increase in parasite cell number and indistinguishable outer cell membranes are indicative of effective exploitation and disguise mechanisms. From 49 dpi onwards, the acute infection changes to a chronic one, with low parasite numbers remaining in the fish. Conclusions To our knowledge, this is the first time myxozoan early development and immune modulation mechanisms have been analyzed along with innate and adaptive immune responses of its fish host, in a controlled laboratory system. Our study adds important information on host–parasite interaction and co-evolutionary adaptation of early metazoans (Cnidaria) with basic vertebrate (fish) immune systems and the evolution of host adaptation and parasite immune evasion strategies. Electronic supplementary material The online version of this article (10.1186/s13071-019-3462-3) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

The kinetics of cellular and humoral immune responses of common carp to presporogonic development of the myxozoan Sphaerospora molnari

et al. 2019

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“…In addition, rainbow trout is often used as a model species for laboratory investigations of fish disease, including to reproduce PKD in controlled conditions [e.g., (14, 17, 18, 23, 34–37)]. Though, rainbow trout and brown trout react differently to T. bryosalmonae infection, in terms of sensitivity to infectious agent and environmental stress (46), intensity of T. bryosalmonae infection (48), or temperature-dependant modulation of the parasite (49) for example. Therefore, some of the conclusions based on experiments with rainbow trout might not correspond to the situation of wild brown trout populations in their natural habitat with fluctuating temperatures.…”

Section: Introductionmentioning

confidence: 99%

Keeping an Eye on Wild Brown Trout (Salmo trutta) Populations: Correlation Between Temperature, Environmental Parameters, and Proliferative Kidney Disease

et al. 2019

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Proliferative kidney disease (PKD) is an emerging disease of salmonids caused by the myxozoan parasite Tetracapsuloides bryosalmonae , which plays a major role in the decrease of wild brown trout ( Salmo trutta ) populations in Switzerland. Strong evidence demonstrated that water temperature modulates parasite infection. However, less knowledge exists on how seasonal water temperature fluctuations influence PKD manifestation under field conditions, how further environmental factors such as water quality may modulate the disease, and whether these factors coalesce with temperatures role possibly giving rise to cumulative effects on PKD. The aims of this study were to (1) determine the correlation between seasonal course of water temperature and PKD prevalence and intensity in wild brown trout populations, (2) assess if other factors such as water quality or ecomorphology correlate with the infection, and (3) quantitatively predict the implication of these factors on PKD prevalence with a statistical model. Young-of-the-year brown trout were sampled in 45 sites through the Canton of Vaud (Switzerland). For each site, longitudinal time series of water temperature, water quality (macroinvertebrate community index, presence of wastewater treatment plant effluent) and ecomorphological data were collected and correlated with PKD prevalence and intensity. 251 T. bryosalmonae -infected trout of 1,118 were found (overall prevalence 22.5%) at 19 of 45 study sites (42.2%). Relation between PKD infection and seasonal water temperature underlined that the mean water temperature for June and the number of days with mean temperature ≥15°C were the most significantly correlated parameters with parasite prevalence and intensity. The presence of a wastewater treatment plant effluent was significantly correlated with the prevalence and infection intensity. In contrast, macroinvertebrate diversity and river ecomorphology were shown to have little impact on disease parameters. Linear and logistic regressions highlighted quantitatively the prediction of PKD prevalence depending on environmental parameters at a given site and its possible increase due to rising temperatures. The model developed within this study could serve as a useful tool for identifying and predicting disease hot spots. These results support the importance of temperature for PKD in salmonids and provides evidence for a modulating influence of additional environmental stress factors.

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“…In Switzerland, elevated water temperatures have been suggested to exacerbate PKD infections and drive disease related mortality of wild brown trout ( Wahli et al, 2002 , 2007 ). Moreover, several lab and field studies have demonstrated the influence of temperature on host-parasite dynamics in the salmonid— T. bryosalmonae system ( Bettge et al, 2009a , 2009b ; Bailey et al, 2017 , 2018 ; Strepparava et al, 2017 ). However, given the strong interference of human activities with the diversity and functioning of freshwater ecosystems ( Søndergaard & Jeppesen, 2007 ; Vörösmarty et al, 2010 ; Dodds, Perkin & Gerken, 2013 ), PKD dynamics may not only be driven by temperature change, but by multiple stressors.…”

Section: Introductionmentioning

confidence: 99%

Do fish get wasted? Assessing the influence of effluents on parasitic infection of wild fish

Bailey

Rubin

Strepparava

et al. 2018

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Many ecosystems are influenced simultaneously by multiple stressors. One important environmental stressor is aquatic pollution via wastewater treatment plant (WWTP) effluents. WWTP effluents may contribute to eutrophication or contain anthropogenic contaminants that directly and/or indirectly influence aquatic wildlife. Both eutrophication and exposure to anthropogenic contaminants may affect the dynamics of fish-parasite systems. With this in mind, we studied the impact of WWTP effluents on infection of brown trout by the parasite Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease (PKD). PKD is associated with the long-term decline of wild brown trout (Salmo trutta) populations in Switzerland. We investigated PKD infection of brown trout at two adjacent sites (≈400 m apart) of a Swiss river. The sites are similar in terms of ecology except that one site receives WWTP effluents. We evaluated the hypothesis that fish inhabiting the effluent site will show greater susceptibility to PKD in terms of prevalence and disease outcome. We assessed susceptibility by (i) infection prevalence, (ii) parasite intensity, (iii) host health in terms of pathology, and (iv) estimated apparent survival rate. At different time points during the study, significant differences between sites concerning all measured parameters were found, thus providing evidence of the influence of effluents on parasitic infection of fish in our study system. However, from these findings we cannot determine if the effluent has a direct influence on the fish host via altering its ability to manage the parasite, or indirectly on the parasite or the invertebrate host via increasing bryozoa (the invertebrate host) reproduction. On a final note, the WWTP adhered to all national guidelines and the effluent only resulted in a minor water quality reduction assessed via standardized methods in this study. Thus, we provide evidence that even a subtle decrease in water quality, resulting in small-scale pollution can have consequences for wildlife.

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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

Cited by 16 publications

References 36 publications

The kinetics of cellular and humoral immune responses of common carp to presporogonic development of the myxozoan Sphaerospora molnari

The kinetics of cellular and humoral immune responses of common carp to presporogonic development of the myxozoan Sphaerospora molnari

Keeping an Eye on Wild Brown Trout (Salmo trutta) Populations: Correlation Between Temperature, Environmental Parameters, and Proliferative Kidney Disease

Do fish get wasted? Assessing the influence of effluents on parasitic infection of wild fish

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