European eel, Anguilla anguilla (Linnaeus) (Elopomorpha: Anguilliformes), is a critically endangered fish of ecological and economic importance, hosting numerous parasites, including myxozoans (Cnidaria). Since its initial discovery in the kidney of European eel, Myxidium giardi Cépède, 1906 has been reported with numerous spore sizes and shapes from various tissues of multiple anguillid species. Morphological variability, wide host and tissue spectrum, and lack of sequence data raised doubts about the conspecificity of reported isolates. Subsequent studies provided 18S rDNA sequences of several isolates from anguillids and other elopiform fish, and demonstrated a split of parasite data into two distinct phylogenetic lineages, one comprising the M. giardi sequence, and the other all species infecting elopiform fishes classified under the recently established genus Paramyxidium Freeman et Kristmundsson, 2018. Myxidium giardi was, however, transferred to this genus as Paramyxidium giardi n. comb. and designated as the type species of the genus. In line with this change, the sequence originally identified as M. giardi was considered to have been incorrectly associated with this species. To shed light on the status of M. giardi originally described by Cépède (1906), we conducted microscopic and molecular examinations of various organs of 24 individuals of European eel, originating from diverse Czech habitats. Through morphometric and molecular analyses, we demonstrated that spore and polar capsule morphology, morphometry and tissue tropism of our European eel kidney parasite isolates matched the features of the original M. giardi description. Our isolates clustered in the lineage encompassing the first published M. giardi sequence. Thus, the originally described M. giardi indeed represents an existing species within the genus Myxidium Bütschli, 1882, which we formally resurrect and redescribe. Due to the morphological and molecular differences between M. giardi and P. giardi of Freeman et Kristmundsson (2018), we additionally rename the latter species as Paramyxidium freemani nom. nov.

Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic

Institute of Hydrobiology Biology Centre Czech Academy of Sciences Ceske Budejovice Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences Ceske Budejovice Czech Republic

Zobrazit více v PubMed

Aguilar A., Alvarez M.F., Leiro J.M., Sanmartin M.L. 2005: Parasite populations of the European eel (Anguilla anguilla L.) in the Rivers Ulla and Tea (Galicia, northwest Spain). Aquaculture 249: 85-94. DOI

Alama-Bermejo G., Hernández-Orts J.S., García-Varela M., Oceguera-Figueroa A., Pecková H., Fiala I. 2023: Diversity of myxozoans (Cnidaria) infecting Neotropical fishes in southern Mexico. Sci. Rep. 13: 12106. DOI

Atkinson S.D., Bartošová-Sojková P., Whipps C.M., Bartholomew J.L. 2015: Approaches for characterising myxozoan species. In: B. Okamura, A. Gruhl and J.L. Bartholomew (Eds.), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, pp. 111-123. DOI

Bartošová P., Fiala I. 2011: Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitol. Res. 108: 573-583. DOI

Bartošová-Sojková P., Hrabcová M., Pecková H., Patra S., Kodádková A., Jurajda P., Tyml T., Holzer A.S. 2014: Hidden diversity and evolutionary trends in malacosporean parasites (Cnidaria: Myxozoa) identified using molecular phylogenetics. Int. J. Parasitol, 44: 565-577. DOI

Bartošová-Sojková P., Lövy A., Reed C.C., Lisnerová M., Tomková T., Holzer A.S., Fiala, I. 2018: Life in a rock pool: radiation and population genetics of myxozoan parasites in hosts inhabiting restricted spaces. PLoS ONE 13: e0194042. DOI

Borgsteede F.H.M., Haenen O.L.M., Deber J., Lisitsina O.I. 1999: Parasitic infections of European eel (Anguilla anguilla, L.) in the Netherlands. Helminthologia 36: 251-260.

Cépède C. 1906: Myxidium giardi Cépède, et la prétendue immunité des Anguilles à l'égard des infections myxosporidiennes. C. R. Séances Soc. Biol. Fil. 6: 170-173.

Chen Q.L., Ma C.L. 1998: Myxozoa, Myxosporea. In: Committee of Fauna Sinica (Ed.), Fauna Sinica. Science Press, Beijing, pp. 292-528.

Copland J.W. 1981: The occurrence and distribution of Myxidium giardi Cépède, 1906 in wild and cultured European eels, Anguilla anguilla L., in England. J. Fish Dis. 4: 231-242. DOI

Copland J.W. 1982: Myxobolus dermatobia (Ishii, 1915) infection of wild eels, Anguilla anguilla L., in England. J. Fish Dis. 5: 549-552. DOI

Dzido J., Rolbiecki L., Izdebska J.N, Bednarek R. 2020: Checklist of the parasites of European eel Anguilla anguilla (Linnaeus, 1758) (Anguillidae) in Poland. Biodivers. Data J. 8: e52346. DOI

Eiras J.C., Saraiva A., Cruz C.F., Santos M.J., Fiala I. 2011: Synopsis of the species of Myxidium Bütschli, 1882 (Myxozoa: Myxosporea: Bivalvulida). Syst. Parasitol. 80: 81-116. DOI

Eszterbauer E., Atkinson S., Diamant A., Morris D., El-Matbouli M., Hartikainen H. 2015: Myxozoan life cycles: practical approaches and insights. In: B. Okamura, A. Gruhl and J.L. Bartholomew (Eds.), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, pp. 175-198. DOI

Fiala I. 2006: The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int. J. Parasitol. 36: 1521-1534. DOI

Fiala I., Bartošová P. 2010: History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evol. Biol. 10: 1-13. DOI

Fiala I., Bartošová-Sojková P., Whipps C.M. 2015: Classification and phylogenetics of Myxozoa. In: B. Okamura, A. Gruhl, and J.L. Bartholomew (Eds.), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, pp. 85-110. DOI

Feunteun E. 2002: Management and restoration of European eel population (Anguilla anguilla): an impossible bargain. Ecol. Eng. 18: 575-591. DOI

Freeman M.A., Kristmundsson Á. 2018: 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). Parasit Vectors 11: 1-13. DOI

Froese R., Pauly D. (Eds) 2023: FishBase. World Wide Web electronic publication. www.fishbase.org, version (10/2023).

Ghittino P., Smith F.G., Glenn J.S. 1974: A case report of Myxosporidia (Myxidium giardi) in the dermis of an American eel (Anguilla rostrata). Riv. Ital. Piscic. Ittiopatol. 9: 13-18.

van Ginneken V.J., Maes G.E. 2005: The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev. Fish Biol. Fish. 15: 367-398. DOI

Grossel G., Handlinger J., Battaglene S., Munday B. 2005: Diagnostic polymerase chain reaction assay to detect Kudoa neurophila (Myxozoa: Multivalvulida) in a marine finfish hatchery. Dis. Aquat. Org. 64: 141-149. DOI

Hallett S.L., Diamant A. 2001: Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n. sp. (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland, Australia. Dis. Aquat. Org. 46: 197-212. DOI

Hartikainen H., Bass D., Briscoe A.G., Knipe H., Green A.J., Okamura B. 2016: Assessing myxozoan presence and diversity using environmental DNA. Int. J. Parasitol. 46: 781-792. DOI

Hillis D.M., Dixon M.T. 1991: Ribosomal DNA: molecular evolution and phylogenetic inference. Q. Rev. Biol. 66: 411-453. DOI

Hine P.M. 1975: Three new species of Myxidium (Protozoa: Myxosporidia) parasitic in Anguilla australis Richardson, 1848 and A. dieffenbachii Gray, 1842 in New Zealand. J. Roy. Soc. New Zealand 5: 153-161. DOI

Hine P.M. 1980: A review of some species of Myxidium Bütschli, 1882 (Myxozosporea) from eels (Anguilla spp.). J. Protozool. 27: 260-267. DOI

Holzer A.S. 2004: Molecular studies on Sphaerospora truttae and other freshwater myxozoans. PhD Thesis, University of Stirling, Stirling, UK, 260 pp.

Holzer A.S., Bartošová P., Pecková H., Tyml T., Atkinson S., Bartholomew J., Sipos D., Eszterbauer E., Dyková I. 2013: 'Who's who' in renal sphaerosporids (Bivalvulida: Myxozoa) from common carp, Prussian carp and goldfish - molecular identification of cryptic species, blood stages and new members of Sphaerospora sensu stricto. Parasitology 140: 46-60. DOI

Holzer A.S., Hartigan A., Patra S., Pecková H., Eszterbauer E. 2014: Molecular fingerprinting of the myxozoan community in common carp suffering Swim Bladder Inflammation (SBI) identifies multiple etiological agents. Parasit. Vectors 7: 1-9. DOI

Holzer A.S., Sommerville C., Wootten R. 2004: Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int. J. Parasitol. 34: 1099-1111. DOI

Holzer A.S., Sommerville C., Wootten R. 2006: Molecular identity, phylogeny and life cycle of Chloromyxum schurovi Shul'man & Ieshko 2003. Parasitol. Res. 99: 90-96. DOI

Ishii S. 1915: Myxosporidiosis of the Japanese eel. Zool. Mag. 27: 372-382.

IUCN 2023: The IUCN Red List of Threatened Species, http://www.iucnredlist.org (accessed 17 October 2023).

Jacob E., Bremen H.B. 1953: Eine bislang unbekannte Sphaerosporose des Flussaals, hervorgerufen durch Sphaerospora reichenowi nova species. Berl. Munch. Tierarztl. Wochenschr. 66: 326-8.

Jakob E., Walter T., Hanel R. 2016: A checklist of the protozoan and metazoan parasites of European eel (Anguilla anguilla): checklist of Anguilla anguilla parasites. J. Appl. Ichthyol. 32: 757-804. DOI

Katoh K., Kuma K.I., Toh H., Miyata T. 2005: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucl. Acids Res. 33: 511-518. DOI

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Drummond A. et al. 2012: Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649. DOI

Kent M.L., Khattra J., Hervio D.M.L., Devlin R.H. 1998: Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora. J. Aquat. Anim. Health 10: 12-21. DOI

Kirk R.S. 2003: The impact of Anguillicola crassus on European eels. Fish. Manag. Ecol. 10: 385-394. DOI

Køie M. 1988: Parasites in European eel Anguilla anguilla (L.) from Danish freshwater, brackish and marine localities. Ophelia 29: 93-118. DOI

Lisnerová M., Blabolil P., Holzer A., Jurajda P., Fiala I. 2020: Myxozoan hidden diversity: the case of Myxobolus pseudodispar Gorbunova, 1936. Folia Parasitol. 67: 019. DOI

Lisnerová M., Holzer A., Blabolil P., Fiala I. 2023: Evaluation and optimization of an eDNA metabarcoding assay for detection of freshwater myxozoan communities. Environ. DNA 5: 312-325. DOI

Lom J., Arthur J.R. 1989: A guideline for the preparation of species descriptions in Myxosporea. J. Fish Dis. 12: 151-156. DOI

Lom J., Dyková I. 2006: Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 53: 1-36. DOI

Lom J., Molnár K., Dyková I. 1986: Hoferellus gilsoni (Debaisieux, 1925) comb. n. (Myxozoa, Myxosporea): redescription and mode of attachment to the epithelium of the urinary bladder of its host, the European eel. Protistologica 22: 405-413.

Miller M.J., Bonhommeau S., Munk P., Castonguay M., Hanel R., McCleave J.D. 2015: A century of research on the larval distributions of the Atlantic eels: a re-examination of the data. Biol. Rev. 90: 1035-1064. DOI

Nagasawa K., Umino T., Mizuno K. 2007: A checklist of the parasites of eels (Anguilla spp.) (Anguilliformes: Anguillidae) in Japan (1915-2007). J. Grad. School Biosphere Sci. 46: 91-121.

Okamura B., Gruhl A., Reft A.J. 2015: Cnidarian origins of the Myxozoa. In: B. Okamura, A. Gruhl and J.L. Bartholomew(Eds.), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, pp. 45-68. DOI

Okamura B., Hartigan A., Naldoni J. 2018: Extensive uncharted biodiversity: the parasite dimension. Integr. Comp. Biol. 58: 1132-1145. DOI

Parzanini C., Arts M.T., Power M., Rohtla M., Skiftesvik A.B., Koprivnikar J., Browman H.I., Milotic D., Durif C.M. 2021: Trophic ecology of the European eel (Anguilla anguilla) across different salinity habitats inferred from fatty acid and stable isotope analysis. Can. J. Fish. Aquat. Sci. 78: 1721-1731. DOI

Posada D. 2008: jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25: 1253-1256. DOI

Ronquist F., Huelsenbeck J.P. 2003: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. DOI

Schneider C.A., Rasband W.S., Eliceiri K.W. 2012: NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9: 671-675. DOI

Sures B., Knopf K., Würtz J., Hirt J. 1999: Richness and diversity of parasite communities in European eels Anguilla anguilla of the River Rhine, Germany, with special reference to helminth parasites. Parasitology 119: 323-330. DOI

Stamatakis A. 2006: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. DOI

Treasurer J.W., Cox D. 1997. The occurrence of Myxidium giardi Cépède, in cultured eels, Anguilla anguilla L., in West Scotland. Bull. Eur. Ass. Fish Pathol. 17: 171-173.

Tuzet O., Ormières R. 1957: Ceratomyxa anguillae n. sp. myxosporidie parasite de la vesicule biliaire des anguilles de l'Etang de Thau. Ann. Parasitol. Hum. Comp. 32: 189-196.

Ventura M.T., Paperna I. 1984: Histopathology of Myxidium giardi Cépède, 1906 infection in European eels, Anguilla anguilla L., in Portugal. Aquaculture 43: 357-368. DOI

Wierzbicka J. 1987: Zschokkella stettinensis sp. n. (Myxospora, Bivalvulida) - a parasite of eel, Anguilla anguilla (L.). Acta Protozool. 26: 79-82.

Yuan Y., Yuan Y., Dai Y., Gong Y., Yuan Y. 2022: Development status and trends in the eel farming industry in Asia. N. Am. J. Aquac. 84: 3-17. DOI

Unraveling the mystery of a myxozoan parasite of the trout: redescription of Chloromyxum schurovi