Molecular fingerprinting of the myxozoan community in common carp suffering Swim Bladder Inflammation (SBI) identifies multiple etiological agents

Abstract

BackgroundSwim bladder inflammation (SBI) is an important disease of common carp fingerlings in Central Europe. In the 1980s, its etiology was ascribed to multicellular proliferative stages of the myxozoan parasite Sphaerospora dykovae (formerly S. renicola). S. dykovae was reported to proliferate in the blood and in the swim bladder prior to the invasion of the kidney, where sporogony takes place. Due to the presence of emerging numbers of proliferative myxozoan blood stages at different carp culture sites in recent years we analysed cases of SBI, for the first time, using molecular diagnostics, to identify the myxozoan parasites present in diseased swim bladders.MethodsWe amplified myxozoan SSU rDNA in a non-specific approach and compared the species composition in swim bladders at culture sites where carp demonstrated 1. No signs of SBI, 2. Minor pathological changes, and 3. Heavy SBI. Based on DNA sequences, we determined the localisation and distribution of the most frequent species by in situ hybridisation, thereby determining which myxozoans are involved in SBI.ResultsLarge multicellular myxozoan swim bladder stages characterised heavy SBI cases and were identified as S. dykovae, however, blood stages were predominantly represented by Sphaerospora molnari, whose numbers were greatly increased in carp with mild and heavy SBI, compared with SBI-free fish. S. molnari was found to invade different organs and cause inflammatory changes also in the absence of S. dykovae. One site with mild SBI cases was characterised by Buddenbrockia sp. infection in different organs and a general granulomatous response.ConclusionsWe provide evidence that the etiology of SBI can vary in relation to culture site and disease severity and that emerging numbers of S. molnari in the blood represent an important co-factor or precondition for SBI.

Transcriptome of Sphaerospora molnari (Cnidaria, Myxosporea) blood stages provides proteolytic arsenal as potential therapeutic targets against sphaerosporosis in common carp

“…The parasites not only use the blood for transport to their target organ but proliferate within it and are present almost all year round ( Fig. 1, [26,28,30]). Sphaerospora molnari is a parasite of the common carp in Central Europe with motile blood stages that provoke a strong immune response [29] and are a likely co-factor for developing Swim Bladder Inflammation [30].…”

Infection dynamics and tissue tropism of Parvicapsula pseudobranchicola (Myxozoa: Myxosporea) in farmed Atlantic salmon (Salmo salar)

“…Molecular evidence has suggested that initial blood stages may occur [ 8 ], as in some other myxosporeans (e.g. [ 16 – 18 ]). Sporogonic stages and spores primarily occur in the pseudobranchs, but have occasionally been detected in other organs in farmed Atlantic salmon, such as the gills, kidney and the liver [ 19 ].…”

New cell motility model observed in parasitic cnidarian Sphaerospora molnari (Myxozoa:Myxosporea) blood stages in fish

“…Intriguingly, before S. molnari produces spores it circulates as a multicellular blood stage in the fish host. These blood stages are termed “extrasporogonic”, they proliferate in the host for months and are associated with swim bladder inflammation16.…”

“…Myxozoan blood stages were first reported in carp in 1976 as “unidentified blood objects”17 and the movement described as “dancing”; only recently SSU rDNA sequencing identified the cells as S. molnari 16. Their dancing movement has also been described as “twitching”18, and is extremely fast, non-directional and produced without tubulin-based cell appendages such as cilia or flagella.…”