pathogens Review The Malacosporean Myxozoan Parasite Tetracapsuloides bryosalmonae: A Threat to Wild Salmonids Arun Sudhagar 1,2, Gokhlesh Kumar 1,* and Mansour El-Matbouli 1 1 Clinical Division of Fish Medicine, University of Veterinary Medicine, Vienna 1210, Austria; [email protected] (A.S.); [email protected] (M.E.-M.) 2 Central Institute of Fisheries Education, Rohtak Centre, Haryana 124411, India * Correspondence: [email protected] Received: 4 November 2019; Accepted: 20 December 2019; Published: 23 December 2019 Abstract: Tetracapsuloides bryosalmonae is a myxozoan parasite responsible for proliferative kidney disease (PKD) in a wide range of salmonids. PKD, characterized by high mortality and morbidity, is well known for affecting aquaculture operations and wild salmonid populations across Europe and North America. The life cycle of T. bryosalmonae revolves around freshwater bryozoan and salmonid fish hosts. In recent years, T. bryosalmonae has been reported among wild salmonids from the European countries where it has not been reported previously. T. bryosalmonae is believed to be a possible reason for the diminishing wild salmonid populations in the natural water bodies of many European countries. Climate crisis driven rising water temperature can further accelerate the distribution of T. bryosalmonae. Expansion of the geographical distribution of T. bryosalmonae may further advocate the decline of wild salmonid populations, especially brown trout (Salmo trutta) in their habitats. Mathematical models are used to understand the pattern and distribution of T. bryosalmonae among the host in the natural water bodies. The present manuscript not only summarizes the incidences of T. bryosalmonae among the wild salmonid populations, but also discusses the contemporary understanding about the development of T. bryosalmonae in its hosts and the influences of various factors in the spread of the disease in the wild. Keywords: brown trout; bryozoan; climate change; myxozoan; proliferative kidney disease 1. Introduction Tetracapsuloides bryosalmonae is a myxozoan parasite belonging to class Malacosporea and is well known for causing proliferative kidney disease (PKD) in salmonids [1]. The parasite life cycle exploits two different host species, an invertebrate bryozoan host and a vertebrate salmonid fish host (Figure1)[ 2–5]. PKD in fish results in the enlargement of kidney and spleen, glomerulonephritis, anemia, ascites, exophthalmia, pale gills and darkened skin in the infected fish depending upon the severity. PKD alone can cause high mortality while secondary infections can speed up the death process and increase mortality even further [6]. T. bryosalmonae poses a serious threat to farmed and wild salmonids across Europe and North America. T. bryosalmonae is one of the major factors associated with the decline of endemic brown trout (Salmo trutta) population in the streams of Alps [7–10]. Pathogens 2020, 9, 16; doi:10.3390/pathogens9010016 www.mdpi.com/journal/pathogens Pathogens 2020, 9, 16 2 of 16 Pathogens 2020, 9, x FOR PEER REVIEW 2 of 14 Figure 1.FigureTetracapsuloides 1. Tetracapsuloides bryosalmonae bryosalmonaelife life cycle cycle in in salmonid salmonid fish fish host host and and invertebrate invertebrate bryozoan bryozoan host host in wild environment.in wild environment. Climate changeClimate associatedchange associated rising waterrising temperaturewater temperature can enhance can enhance the proliferation the proliferation of the parasite in both hosts. Waterfowls are suspected to be the long-distance vector of of the parasite in both hosts. Waterfowls are suspected to be the long-distance vector of the parasite. the parasite. In recentIn recent years, yearsT. bryosalmonae, T. bryosalmonaehas has been been reportedreported from from new new geographical geographical locations locations from wild from wild salmonids.salmonids. This canThis be can due be due to theto the spread spread of of the the parasiteparasite to to new new locations locations or due or to due the toemergence the emergence of of PKD outbreaksPKD outbreaks by the by already the already existing existing parasite parasite in thatin that aquatic aquatic ecosystem ecosystem unnoticed unnoticed forfor aa longlong period. However,period.T. bryosalmonae However, T. bryosalmonaeincidences areincidences threatening are threatening as it can as lead it can to lead massive to massive fish killfish eventskill events in natural in natural water bodies affecting endemic fish population. T. bryosalmonae was responsible for the water bodies affecting endemic fish population. T. bryosalmonae was responsible for the mass mortality mass mortality of salmonids, particularly wild mountain whitefish (Prosopium williamsoni) from the of salmonids,Yellowstone particularly river, Montana, wild mountain USA [11]. This whitefish incidence (Prosopium led to thewilliamsoni shutdown of) from300 km the river Yellowstone segment river, Montana,to USApublic[ 11access]. This for incidencea certain period led to of the time, shutdown which subsequently of 300 km riveraffected segment local tourism to public and accessthe for a certainassociated period of economy time, which [12]. It subsequently is important to a ffhighlightected local that tourismhigh-water and temperature the associated and low economy water [12]. It is importantflow cognate to highlight with this fish that kill high-water incidence. temperature and low water flow cognate with this fish kill incidence.The impact of T. bryosalmonae parasite on the protracted decline of wild fish populations is often more challenging to study as the infection dynamics is influenced by rising water temperature The impact of T. bryosalmonae parasite on the protracted decline of wild fish populations is often related to emerging climate change. Laboratory experiments depict that rising water temperature more challengingcan enhance to parasite study production as the infection in both dynamics bryozoan and is influenced fish host [13 by–16] rising. Moreover, water salmonids temperature are related to emergingcold water climate fish change. that are Laboratorysensitive to higher experiments temperatures, depict which that may rising further water aggravate temperature the disease can enhance parasitecondition production in the in wild. both Juvenile bryozoan and and adult fish salmonids host [13 –prefe16].r Moreover,to occupy streams salmonids with aretemperature cold water fish that areranging sensitive between to higher 13–18 temperatures, °C and the water which temperature may further approximately aggravate theabove disease 23–25 condition°C is fatal infor the wild. salmonids [17]. Researchers also suspect waterfowl and common carp for the spread of T. Juvenile and adult salmonids prefer to occupy streams with temperature ranging between 13–18 ◦C bryosalmonae to naive locations. This review discusses about the T. bryosalmonae development in its and thehost, water emerging temperature incidences approximately of the parasite, above role of 23–25 climat◦eC change is fatal and for the salmonids biological vectors [17]. Researchers that also suspectenhances waterfowl the spread and of the common parasite among carp for wild the salmonids. spread of T. bryosalmonae to naive locations. This review discusses about the T. bryosalmonae development in its host, emerging incidences of the parasite, role of climate2. Tetracapsuloides change and bryosalmonae the biological vectors that enhances the spread of the parasite among wild salmonids.Despite the fact that PKD like condition was first described in early 1920’s from Germany in rainbow trout (Oncorhynchus mykiss) [18], the disease condition was named as proliferative kidney 2. Tetracapsuloidesdisease in early bryosalmonae 1970’s defining the main clinical features [19]. Transmission electron microscopic studies in 1985 revealed that a myxozoan parasite is the causative agent of PKD [20]. In the late Despite1990s, the involvement fact that PKD of an like invertebrate condition bryozoan was first host described was discovered in early in the 1920’s life cycle from of Germany this in rainbow trout (Oncorhynchus mykiss)[18], the disease condition was named as proliferative kidney disease in early 1970’s defining the main clinical features [19]. Transmission electron microscopic studies in 1985 revealed that a myxozoan parasite is the causative agent of PKD [20]. In the late 1990s, the involvement of an invertebrate bryozoan host was discovered in the life cycle of this myxozoan parasite [21]. The parasite was taxonomically distinguished from Buddenbrockia sp. and Pathogens 2020, 9, 16 3 of 16 eventually named as Tetracapsuloides bryosalmonae under a new myxozoan class malacosporea [1,22,23]. Molecular phylogenetic studies suggest that myxozoans are evolutionarily primitive, morphologically degenerated cnidarians and their polar capsules are comparable with cnidarians nematocyst [24]. Two clades of T. bryosalmonaePathogens 2020, 9, x stemmingFOR PEER REVIEW from North America and Europe were identified. Interestingly,3 of 14 the North Americanmyxozoan clade parasite of parasites [21]. The parasite was isolated was taxonomically from southern distinguished Europe. from Buddenbrockia Scientific evidencesp. and suggests aquatic birdseventually to be the named possible as Tetracapsuloides vector for transportingbryosalmonae under the a parasite new myxozoan between class the malacosporea continents [25]. The freshwater[1,22,23]. Molecular bryozoan phylogenetic acts