Studies of Myxidium giardi Cépède, 1906 infections in Icelandic eels identifies a genetically diverse clade of myxosporeans that represents the Paramyxidium n. g. (Myxosporea: Myxidiidae)

Abstract

BackgroundThe myxosporean Myxidium giardi Cépède, 1906 was described infecting the kidney of the European eel, Anguilla anguilla (L.), having spindle-shaped myxospores and terminal sub-spherical polar capsules. Since then, numerous anguillid eels globally have been documented to have similar Myxidium infections. Many of these have been identified using the morphological features of myxospores or by the location of infection in the host, and some have been subsequently synonymised with M. giardi. Therefore, it is not clear whether M. giardi is a widely distributed parasite, infecting numerous species of eels, in multiple organs, or whether some infections represent other, morphologically similar but different species of myxosporeans. The aim of the present study was to assess the status of M. giardi infections in Icelandic eels, and related fish hosts in Malaysia and to use spore morphology and molecular techniques to evaluate the diversity of myxosporeans present.ResultsThe morphologies of the myxospores from Icelandic eels were very similar but the overall dimensions were significantly different from the various tissue locations. Myxospores from the kidney of the Malaysian tarpon, Megalops cyprinoides (Broussonet), were noticeably smaller. However, the SSU rDNA sequences from the different tissues locations in eels, were all very distinct, with percentage similarities ranging from 92.93% to as low as 89.8%, with the sequence from Malaysia being even more dissimilar. Molecular phylogenies consistently placed these sequences together in a clade that we refer to as the Paramyxidium clade that is strongly associated with the Myxidium clade (sensu stricto). We erect the genus Paramyxidium n. g. (Myxidiidae) to accommodate these histozoic taxa, and transfer Myxidium giardi as Paramyxidium giardi Cépède, 1906 n. comb. as the type-species.ConclusionsThere is not a single species of Myxidium (M. giardi) causing systemic infections in eels in Iceland. There are three species, confirmed with a robust phylogeny, one of which represents Paramyxidium giardi n. comb. Additional species probably exist that infect different tissues in the eel and the site of infection in the host fish is an important diagnostic feature for this group (Paramyxidium n. g. clade). Myxospore morphology is generally conserved in the Paramyxidium clade, although actual spore dimensions can vary between some species. Paramyxidium spp. are currently only known to infect fishes from the Elopomorpha.

A novel histozoic myxosporean, Enteromyxum caesio n. sp., infecting the redbelly yellowtail fusilier, Caesio cuning, with the creation of the Enteromyxidae n. fam., to formally accommodate this commercially important genus

“…Although myxospore morphology is well conserved within the Enteromyxum clade, the four described species are genetically divergent sharing only between 82.2%–88.7% identity to each other with respect to SSU rDNA sequences. This phenomenon has been reported before, where a robustly supported clade of myxosporeans, the Paramyxidium , has a highly conserved myxospore morphology but a broad genetic diversity ( Freeman & Kristmundsson, 2018 ). For the Paramyxidium , it has been suggested that this is due to a significant under-sampling of species within the genus/clade and that many more members of the Paramyxidium will be uncovered with more extensive molecular sampling ( Fiala et al, 2019 ).…”

Molecular data infers the involvement of a marine aurantiactinomyxon in the life cycle of the myxosporean parasite Paramyxidium giardi (Cnidaria, Myxozoa)

“…This finding is corroborated by the experimental transmission study performed by Benajiba and Marques (1993), who also identified the actinosporean counterpart of P. giardi as an aurantiactinomyxon type, but developing in a freshwater tubificid. Accordingly, Freeman and Kristmundsson (2018) suggested freshwater oligochaetes as the most probable annelid hosts of Paramyxidium spp., considering that known fish hosts [European eel and Indo-Pacific tarpon Megalops cyprinoides (Broussonet, 1782)], were sampled from freshwater habitats. Nonetheless, both these species are migratory fish that spawn at sea producing leptocephalic larvae that migrate into inland waters to grow.…”

“…The genus Paramyxidium Freeman and Kristmundsson, 2018 encompasses species that, whilst being morphologically similar to Myxidium , differ by having histozoic development in various tissues of fish from Elopomorpha (see Freeman and Kristmundsson, 2018). The European eel is the sole representative of Elopomorpha in Portuguese waters.…”

“…Thus far, it has been recognized to host four myxosporean species in this geographic location, including P. giardi from infections that occur in multiple organs (Ventura and Paperna, 1984; Azevedo et al ., 1989; Saraiva and Chubb, 1989; Saraiva and Eiras, 1996; Hermida et al ., 2008). The study by Freeman and Kristmundsson (2018), however, showed that P. giardi is not systemic; while myxospore morphology is conserved and, therefore, unreliable for identification at the species-level, the site of infection appears to be an important diagnostic feature for the group. As such, it is expected that the myxozoan survey of A. anguilla in Portuguese Rivers will lead to the discovery of other Paramyxidium spp.…”

“…In turn, both tetractinomyxon types were described from marine polychaetes, Hediste diversicolor (Müller, 1776) and an undetermined species of Capitella Blainville, 1828, and molecularly shown to be involved in the life cycle of Ellipsomyxa mugilis (Sitjà-Bobadilla and Alvarez-Pellitero, 1993) from the gall bladder of grey mullets and Sphaerospora dicentrarchi Sitjà-Bobadilla and Alvarez-Pellitero, 1992 from systemic infections in D. labrax , respectively (Rangel et al ., 2009, 2016 b ). To our best knowledge, further 17 myxosporean species have been reported from fishes inhabiting Portuguese rivers and estuaries, including Paramyxidium giardi (Cépède, 1906) Freeman and Kristmundsson, 2018 (see Eiras, 2016).…”