Morphological, histological and molecular characterization of Myxobolus kingchowensis and Thelohanellus cf. sinensis infecting gibel carp Carassius auratus gibelio (Bloch, 1782)
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Bo Zhang
Abstract
A Myxobolus species and a Thelohanellus species infecting Carassius auratus gibelio (Bloch, 1782) were redescribed by their morphological, histological and molecular characterization. In the present study, the Myxobolus species infecting the muscle was identified as Myxobolus kingchowensisChen et Ma, 1998 by the morphological and molecular data. Histologically, mature spores of M. kingchowensis were observed in the intercellular and connective tissue of muscle, though the plasmodia were not found. In addition, scattered spores also occurred in the intercellular of haematopoietic cells, intraepithelial of the renal tubules and interior of the melano-macrophage centres. Phylogenetic analysis showed that M. kingchowensis clustered in the clade of muscle-infecting Myxobolus species, further supporting muscle as the infection site of M. kingchowensis. The present Thelohanellus species infecting the gills was identified conspecific as Thelohanellus sinensis reported in Sun (2006) (mark it as T. sinensis-Sun)based on spore morphology, biological traits (host specificity and organ specificity), and molecular data. However, compared with the original description of T. sinensisChen et Hsieh, 1960, the present Thelohanellus species and T. sinensis-Sun both infecting the gills of gibel carp are distinguishable from the original description in the host and infection site, which made the validity of T. sinensis-Sun dubious. Due to the absence of molecular data in the original description of T. sinensis, we suggest marking the present species and T. sinensis-Sun as T. cf. sinensis to avoid the confusion until T. sinensis is obtained from the type host and type infection site.
Acknowledgement
We would like to thank Zizhen Wu for samples collection. This study was supported by the Nature Science Foundation of China (Project Number 31501848, 31572233), China Agriculture Research System (CARS-46) and Demonstration of Key Techniques for High Quality Aquatic Products (Project Number 2016620000001046).
References
Atkinson S.D., Bartošová-Sojková P., Whipps C.M., Bartholomew J.L. 2015. Approaches for characterising myxozoan species. (Eds B. Okamura, A. Gruhl, J. L. Bartholomew) Myxozoan Evolution, Ecology and Development, Cham, Springer. pp. 111–123. https://doi.org/10.1007/978-3-319-14753-6_610.1007/978-3-319-14753-6_6Search in Google Scholar
Chen C.L. 1973. An illustrated guide to the fish diseases and causative pathogenic fauna and flora in the Hubei Province. Inst. Hydrobiol., Publishing House Science, Beijing, China. (In Chinese)Search in Google Scholar
Chen C.L., Hsieh S.R. 1960. Studies on sporozoa from the freshwater fishes Ophiocephalus maculatus and O. argus of China. Actc Hydrobiologica Sinica, 2, 171–196Search in Google Scholar
Chen Q.L., Ma C.L. 1998. Myxozoa: Myxosporea. Science Press, Beijing. (In Chinese)Search in Google Scholar
Darriba D., Taboada G.L., Doallo R., Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772–772. 10.1038/nmeth.2109Search in Google Scholar PubMed PubMed Central
Dereeper A., Audic S., Claverie J.-M., Blanc G. 2010. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evolutionary Biology, 10, 8. https://doi.org/10.1186/1471-2148-10-810.1186/1471-2148-10-8Search in Google Scholar PubMed PubMed Central
Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., et al. 2008. Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research, 36, W465-W469. https://doi.org/10.1093/nar/gkn18010.1093/nar/gkn180Search in Google Scholar PubMed PubMed Central
Drummond A.J., Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214. https://doi.org/10.1186/1471-2148-7-21410.1186/1471-2148-7-214Search in Google Scholar PubMed PubMed Central
Eiras J.C., Molnár K., Lu Y.S. 2005. Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology, 61, 1–46. 10.1007/s11230-004-6343-9Search in Google Scholar PubMed
Fiala I., Bartošová-Sojková P., Whipps C.M. 2015. Classification and phylogenetics of Myxozoa. (Eds B. Okamura, A. Gruhl, J. L. Bartholomew) Myxozoan Evolution, Ecology and Development, Cham, Springer. pp. 85–110. https://doi.org/10.1007/978-3-319-14753-6_510.1007/978-3-319-14753-6_5Search in Google Scholar
Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. 10.1093/sysbio/syq010Search in Google Scholar PubMed
Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. 10.1080/10635150390235520Search in Google Scholar PubMed
Hartigan A., Wilkinson M., Gower D.J., Streicher J.W., Holzer A.S., Okamura B. 2016. Myxozoan infections of caecilians demonstrate broad host specificity and indicate a link with human activity. International Journal for Parasitology, 46, 375–381. https://doi.org/10.1016/jijpara.2016.02.00110.1016/j.ijpara.2016.02.001Search in Google Scholar PubMed
Hillis D.M., Dixon M.T. 1991. Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology, 66, 411–453. https://doi.org/10.1086/41733810.1086/417338Search in Google Scholar PubMed
Katoh K., Standley D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. 10.1093/molbev/mst010Search in Google Scholar PubMed PubMed Central
Kent M.L., Bagshaw J.W., Nener J., Raymond B. 1996. Myxobolus cyprini Doflein, 1898, in Peamouth: First Report of This Myxosporean in the Western Hemisphere. Journal of Aquatic Animal Health, 8, 159–162. 10.1577/1548-8667 (1996) 008< 0159: MCDIPF>2.3.CO;2Search in Google Scholar
Liu Y., Zhai Y.H., Gu Z.M. 2016b. Morphological and molecular characterization of Thelohanellus macrovacuolaris n. sp. Myxosporea: Bivalvulida infecting the palate in the mouth of common carp Cyprinus carpio L. in China. Parasitology International, 65, 303–307. https://doi.org/10.1016/j.parint.2016.02.01310.1016/j.parint.2016.02.013Search in Google Scholar PubMed
Lom J., Arthur J. 1989. A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12, 151–156. 10.1111/j.1365-2761.1989.tb00287.xSearch in Google Scholar
Maciel P.O., Affonso E.G., Boijink C.D.L., Tavaresdias M., Inoue L.A.K.A. 2011. Myxobolus sp. (Myxozoa) in the circulating blood of Colossoma macropomum (Osteichthyes, Characidae). Revista Brasileira De Parasitologia Veterinaria, 20, 82–84. 10.1590/S1984-29612011000100018Search in Google Scholar
Molnár K. 1994. Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitology Hung, 27, 5–20Search in Google Scholar
Molnár K. 2011. Remarks to the validity of Genbank sequences of Myxobolus spp. Myxozoa, Myxosporidae infecting Eurasian fishes. Acta Parasitologica, 56, 263. https://doi.org/10.2478/s11686-011-0054-610.2478/s11686-011-0054-6Search in Google Scholar
Molnár K., Eszterbauer E. 2015. Specificity of infection sites in vertebrate hosts. In: (Eds B. Okamura, A. Gruhl, J. L. Bartholomew) Myxozoan Evolution, Ecology and Development, Cham, Springer. pp. 295–313. https://doi.org/10.1007/978-3-319-14753-6_1610.1007/978-3-319-14753-6_16Search in Google Scholar
Molnár K., Kovács-Gayer É. 1985. The pathogenicity and development within the host fish of Myxobolus cyprini Doflein, 1898. Parasitology, 90, 549–555. 10.1017/S0031182000055530Search in Google Scholar
Ronquist F., Teslenko M., Van Der Mark P., Ayres D.L., Darling A., Höhna S., et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys02910.1093/sysbio/sys029Search in Google Scholar PubMed PubMed Central
Sun C.Y. 2006. Morphological and molecular comparison of myxosporeans. Master Thesis, Chong Qing Normal University, Chongqing, China. (In Chinese)Search in Google Scholar
Whipps C.M., Adlard R.D., Bryant M.S., Lester R.J., Findlay V., Kent M.L. 2003. First report of three Kudoa species from eastern Australia: Kudoa thyrsites from mahi mahi Coryphaena hippurus, Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper Pempheris ypsilychnus. Journal of Eukaryotic Microbiology, 50, 215–219. 10.1111/j.1550-7408.2003.tb00120.xSearch in Google Scholar PubMed
Yuan S., Xi B., Wang J., Xie J., Zhang J. 2015. Thelohanellus wangi n. sp. Myxozoa, Myxosporea, a new gill parasite of allogynogenetic gibel carp Carassius auratus gibelio Bloch in China, causing severe gill myxosporidiosis. Parasitology Research, 114, 37–45. https://doi.org/10.1007/s00436-014-4157-510.1007/s00436-014-4157-5Search in Google Scholar PubMed
Zhang J.Y., Gu Z.M., Kalavati C., Eiras J.C., Liu Y., Guo Q.Y., et al. 2013. Synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Systematic Parasitology, 86, 235–256. 10.1007/s11230-013-9449-0Search in Google Scholar PubMed
© 2018 W. Stefański Institute of Parasitology, PAS
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Articles in the same Issue
- Morphological, histological and molecular characterization of Myxobolus kingchowensis and Thelohanellus cf. sinensis infecting gibel carp Carassius auratus gibelio (Bloch, 1782)
- Cystic echinococcosis in animals and humans of Maharashtra State, India
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- Molecular cloning of enolase from Trichinella spiralis and the protective immunity in mice
- A new species of Cacatuocotyle (Monogenea, Dactylogyridae) parasitizing Astyanax spp. (Characiformes, Characidae) from Brazil, including molecular data and a key to species identification
- Entamoeba histolytica L220 induces the in vitro activation of macrophages and neutrophils and is modulated by neurotransmitters
- Characterization of the complete mitochondrial genome of Metastrongylus salmi (M. salmi) derived from Tibetan pigs in Tibet, China
- Balantioides coli: morphological and ultrastructural characteristics of pig and non-human primate isolates
- Genetic diversity of Taenia hydatigena in the northern part of the West Bank, Palestine as determined by mitochondrial DNA sequences
- Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region
- Histological description of Cercaria etgesiiShchenkov, 2017 daughter sporocysts (Trematoda: Pleurogenidae): compartmentalization of the brood cavity and germinal mass morphology
- Isolation, identification and characterization of the nematophagous fungus Arthrobotrys (Monacrosporium) sinense from China
- First molecular characterization and morphological aspects of Sarcocystis fusiformis infecting water buffalo Bubalus bubalis in Egypt
- Prevalence and risk factors associated with Tritrichomonas foetus infection in cattle in the state of Paraíba, Brazil
- The development of Neoechinorhynchus buttnerae (Eoacanthocephala: Neoechinorhynchidae) in its intermediate host Cypridopsis vidua in Brazil
- Primary culture of cat intestinal epithelial cells in vitro and the cDNA library construction
- Evaluation of the protective effect of a prime-boost strategy with plasmid DNA followed by recombinant adenovirus expressing BmAMA1 as vaccines against Babesia microti infection in hamster
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- Presence of Acanthamoeba in the ocular surface in a Spanish population of contact lens wearers
- Genotyping and virulence analysis of Toxoplasma gondii isolates from a dead human fetus and dead pigs in Jiangsu province, Eastern China
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- Detection of Dirofilaria immitis antigen and antibodies against Anaplasma phagocytophilum, Borrelia burgdorferi and Ehrlichia canis in dogs from ten provinces of China
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- Case report
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- Case report
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