Myxobolus opsaridiumi sp. nov. (Cnidaria: Myxosporea) infecting different tissues of an ornamental fish, Opsaridium ubangiensis (Pellegrin, 1901), in Cameroon: morphological and molecular characterization
Abstract
We report a new myxozoan, Myxobolus opsaridiumi sp. nov., infecting the ornamental fish Opsaridium ubangiensis (Pellegrin, 1901) collected from the Anga River near the city of Yaounde, Cameroon. Plasmodia were found in the skin, muscles and spleen. The overall prevalence of infection was 54.7% (288 parasitized fish out of 526 examined). The myxospores were ovoid to subspherical in frontal view and lenticular in lateral view. The valves were symmetrical and relatively thick, without edge markings. The myxospore measurements were 10.7 ± 0.14 (10–11.5) μm long, 9 ± 0.15 (8–10) μm wide and 6.2 ± 0.7 (5.6–7.2) μm thick. The two ovoid polar capsules were equal in size, converging and opening together at the anterior end, measuring 5 ± 0.07 (4.3–6.0) μm long and 2.7 ± 0.07 (2.2–3.0) μm wide. Polar filaments were coiled from 5 to 7 turns. Histopathological analysis revealed no inflammatory reaction associated with the infection. A BLAST search found that the newly obtained 18 rDNA sequence had a low sequence similarity with available sequences for Myxobolus on GenBank. A phylogenetical analysis based on ribosomal DNA partial sequences showed that M. opsaridiumi sp. nov. is closely associated with several species of Myxobolus infecting cyprinid fish.
References
Abakar-Ousman A., Fomena P., Ngassam & Bouix G. 2006. Myxosporidian (Myxozoa) parasites of fresh water fish teleostean from Chad: new or few known species. Annales de l’Université de N’Djamena, Ser. C 1: 111–121.
Agius C. & Roberts R.J. 2003. Melano‐macrophage centres and their role in fish pathology. Journal of Fish Diseases 26: 499–509. https://doi.org/10.1046/j.1365-2761.2003.00485.x
Ali M.A., Al-Rasheid K.A., Sakran T., Abdel-Baki A.-A. & Abdel-Ghaffar F.A. 2002. Some species of the genus Myxobolus (Myxozoa: Myxosporea) infecting freshwater fish of the River Nile, Egypt, and the impact on their hosts. Parasitology Research 88: 9–15. https://doi.org/10.1007/s004360100449
Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W. & Lipman D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25 (17): 3389–3402. https://doi.org/10.1093/nar/25.17.3389
Atkinson S.D., Bartholomew J.L. & Lotan T. 2018. Myxozoans: Ancient metazoan parasites find a home in phylum Cnidaria. Zoology (Jena) 129: 66–68.
Baska F. 1987. Histological studies on the development of Myxobolus pseudodispar Gorbunova, 1936 in the roach (Rutilus rutilus). Acta Veterinaria Hungarica 35: 251–257.
Basu S. & Haldar D. 2003. Three new species of Myxobolus Butschli, 1882 from different food fishes of West Bengal, India. Acta Protozoologica 42: 245–251.
Boungou M., Kabre G.B., Sakiti N.G., Marques A. & Sawadogo L. 2006. Description of four new myxosporean species (Myxozoa: Myxosporea) from genus Myxobolus, fish parasites of Burkina Faso, West Africa. Journal of Biological Sciences 6 (5): 861–867.
Deli A., Lekeufack F.G.B. & Abraham F. 2017. Description of Myxidium tetraodoni sp. nov., Myxidium anisocapsularis sp. nov. and Myxobolus magai sp. nov. (Myxosporea: Bivalvulida) infecting some freshwater fishes in Cameroon (Central Africa). Fisheries and Aquaculture Journal 8 (4): 1–11. https://doi.org/10.4172/2150-3508.1000235
Dyková I. 1984. The role of melanomacrophage centres in the tissue reaction to myxosporean infections of fishes. Bulletin of the European Association of Fish Pathologists 4 (4): 65.
Dyková I. & Lom J. 2007. Histopathology of Protistan and Myxozoan Infections in Fishes. An Atlas. Academia, Prague.
Eiras J.C., Molnár K. & Lu Y.S. 2005. Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology 61 (1): 1–46. https://doi.org/10.1007/s11230-004-6343-9
Eiras J.C., Monteiro C.M & Brasil-Sato M.C. 2010. Myxobolus franciscoi sp. nov. (Myxozoa: Myxosporea: Myxobolidae), a parasite of Prochilodus argenteus (Actinopterygii: Prochilodontidae) from the Upper São Francisco River, Brazil, with a revision of Myxobolus spp. from South America. Zoologia (Curitiba) 27 (1): 131–137.
Eiras J.C., Zhang J. & Molnár K. 2014. Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea, Myxobolidae) described between 2005 and 2013. Systematic Parasitology 88 (1): 11–36. https://doi.org/10.1007/s11230-014-9484-5
Fiala I. 2006. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36: 1521–1534. https://doi.org/10.1016/j.ijpara.2006.06.016
Fiala I., Bartošová-Sojková P., Okamura B. & Hartikainen H. 2015. Adaptive radiation and evolution within the Myxozoa. In: Okamura B., Gruhl A. & Bartholomew J.L. (eds) Myxozoan Evolution, Ecology and Development: 69–84. Springer International Publishing, Cham, Switzerland.
Gilman M.M. & Eiras J.C. 1998. Kudoa sp. (Myxosporea, Multivalvulida) infecting Sardina pilchardus (Walb., 1792) off the Portuguese coast. Research and Reviews in Parasitology 58 (2): 135–137.
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 (3): 307–321. https://doi.org/10.1093/sysbio/syq010
Haldar D.P., Das M.K. & Sharma B.K. 1983. Studies on protozoan parasites from fishes: four new species of the genera Henneguya Thélohan, 1892, Thelohanellus Kudo, 1933, and Myxobolus Bütschli, 1892. Archiv für Protistenkunde 127 (3): 283–296. https://doi.org/10.1016/S0003-9365(83)80023-2
Holzer A.S., Bartošová-Sojková P., Born-Torrijos A., Lövy A., Hartigan A. & Fiala I. 2018. The joint evolution of the Myxozoa and their alternate hosts: a cnidarian recipe for success and vast biodiversity. Molecular Ecology 27 (7): 1651–1666. https://doi.org/10.1111/mec.14558
Jiménez-Guri E., Okamura B. & Holland P.W. 2007. Origin and evolution of a myxozoan worm. Integrative and Comparative Biology 47 (5): 752–758. https://doi.org/10.1093/icb/icm026
Karlsbakk E., Kristmundsson A., Albano M., Brown P. & Freeman M.A. 2017. Redescription and phylogenetic position of Myxobolus aeglefini and Myxobolus platessae n. comb. (Myxosporea), parasites in the cartilage of some North Atlantic marine fishes, with notes on the phylogeny and classification of the Platysporina. Parasitology International 66 (1): 952–959. https://doi.org/10.1016/j.parint.2016.10.014
Kaur H. & Singh R. 2012. A synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Bivalvulida) parasitising Indian fishes and a revised dichotomous key to myxosporean genera. Systematic Parasitology 81 (1): 17–37. https://doi.org/10.1007/s11230-011-9321-z
Kent M.L., Andree K.B., Bartholomew J.L., El-Matbouli M., Desser S.S., Devlin R.H., Feist S.W., Hedrick R.P., Hoffmann R.W., Khattra J., Hallett S.L., Lester R.J., Longshaw M., Palenzeula O., Siddall M.E. & Xiao C. 2001. Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48 (4): 395–413. https://doi.org/10.1111/j.1550-7408.2001.tb00173.x
Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J. & Higgins D.G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23 (21): 2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Lekeufack F.G.B. & Fomena A. 2013. Structure et dynamique des infracommunautés de myxosporidies parasites de Ctenopoma petherici Günther, 1864 (Anabantidae), Clarias pachynema Boulenger, 1903 (Clariidae) et Hepsetus odoe (Bloch, 1794) (Hepsetidae) dans la rivière Sangé au Cameroun. International Journal of Biological and Chemical Sciences 7 (6): 2301–2316. https://doi.org/10.4314/ijbcs.v7i6.11
Lekeufack F.G.B., Abdel-Baki A.S., Ateba N.O.O., Fomena A. & Mansour L. 2019. Morphological and molecular characterization of Myxobolus dibombensis sp. n. (Myxozoa: Myxobolidae), a parasite of the African carp Labeo barbus batesii (Teleostei: Cyprinidae) from Dibombe River, Cameroon. Parasitology Research 118: 763–771. https://doi.org/10.1007/s00436-019-06209-w
Lisnerová M., Blabolil P., Holzer A., Jurajda P. & Fiala I. 2020. Myxozoan hidden diversity: the case of Myxobolus pseudodispar Gorbunova, 1936. Folia Parasitologica (Praha) 67: e019. https://doi.org/10.14411/fp.2020.019
Liu X.H., Batueva M.D., Zhao Y.L., Zhang J.Y., Zhang Q.Q., Li T.T. & Li A.H. 2016. Morphological and molecular characterisation of Myxobolus pronini n. sp. (Myxozoa: Myxobolidae) from the abdominal cavity and visceral serous membranes of the gibel carp Carassius auratus gibelio (Bloch) in Russia and China. Parasites & Vectors 9: e562. https://doi.org/10.1186/s13071-016-1836-3
Liu Y., Lövy A., Gu Z. & Fiala I. 2019. Phylogeny of Myxobolidae (Myxozoa) and the evolution of myxospore appendages in the Myxobolus clade. International Journal for Parasitology 49 (7): 523–530. https://doi.org/10.1016/j.ijpara.2019.02.009
Lom J. & Arthur J.R. 1989. A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12: 151–156. https://doi.org/10.1111/j.1365-2761.1989.tb00287.x
Lom J. & Dykova I. 2006. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica (Praha) 53: 1–36. https://doi.org/10.14411/fp.2006.001
Longshaw M., Frear P. & Feist S.W. 2003. Myxobolus buckei sp. n. (Myxozoa), a new pathogenic parasite from the spinal column of three cyprinid fishes from the United Kingdom. Folia Parasitologica (Praha) 50: 251–262. https://doi.org/10.14411/fp.2003.043
Mandour A., Galal A. & Abed G. 1993. Myxobolus clarii n. sp. in the testis of the fish Clarias lazera from the River Nile of Assiut [Egypt]. Assiut Veterinary Medical Journal 29 (58): 108–114.
Manrique W.G., Figueiredo M.A.P., de Andrade Belo M.A., Martins M.L. & de Moraes F.R. 2015. First report of Myxobolus sp. infection in the skeletal muscle of Neotropical freshwater fish Piaractus mesopotamicus. Parasitology Research 114: 2041–2044. https://doi.org/10.1007/s00436-015-4454-7
Mansour L., Thabet A., Chourabi K., Harrath A.H., Gtari M., Al Omar S.Y. & Ben Hassine O.K. 2013. Kudoa azevedoi n. sp. (Myxozoa, Multivalvulida) from the oocytes of the Atlantic horse mackerel Trachurus trachurus (Perciformes, Carangidae) in Tunisian coasts. Parasitology Research 112 : 1737–1747. https://doi.org/10.1007/s00436-013-3332-4
Mansour L., Harrath A.H., Abd-Elkader O.H., Alwasel S., Abdel-Baki A.A.S. & Al Omar S.Y. 2014. Structural and molecular characterization of Kudoa quraishii n. sp. from the trunk muscle of the Indian mackerel Rastrelliger kanagurta (Perciforme, Scombridae) in Saudi Arabia coasts. Parasitology Research 113: 1361–1370. https://doi.org/10.1007/s00436-014-3775-2
Mathews P.D., Mertins O., Milanin T., Espinoza L.L., Flores-Gonzales A.P., Audebert F. & Morandini A.C. 2020. Molecular phylogeny and taxonomy of a new Myxobolus species from the endangered ornamental fish, Otocinclus cocama endemic to Peru: a host-parasite coextinction approach. Acta Tropica 210: e105545. https://doi.org/10.1016/j.actatropica.2020.105545
Molnár K. 1994. Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitologia Hungarica 27: 5–20.
Molnár K. & Székely C. 2014. Tissue preference of some myxobolids (Myxozoa: Myxosporea) from the musculature of European freshwater fishes. Diseases of Aquatic Organisms 107: 191–198. https://doi.org/10.3354/dao02688
Molnár K., Eszterbauer E., Székely C., Dan A. & Harrach B. 2002. Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. Journal of Fish Diseases 25: 643– 652. https://doi.org/10.1046/j.1365-2761.2002.00409.x
Molnár K., Székely C., Hallett S.L. & Atkinson S.D. 2009. Some remarks on the occurrence, host-specificity and validity of Myxobolus rotundus Nemeczek, 1911 (Myxozoa: Myxosporea). Systematic Parasitology 72 (1): 71–79. https://doi.org/10.1007/s11230-008-9161-7
Molnar K., Cech G. & Székely C. 2011. Histological and molecular studies of species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea) in the gills of Abramis, Blicca and Vimba spp. (Cyprinidae), with the redescription of M. macrocapsularis Reuss, 1906 and M. bliccae Donec & Tozyyakova, 1984. Systematic Parasitology 79 (2): 109–121. https://doi.org/10.1007/s11230-011-9292-0
Ogawa K., Delgahapitiya K.P., Furuta T. & Wakabayayashi H. 1992. Histological studies on the host response to Myxobolus artus Akhmerov, 1960 (Myxozoa: Myxobolidae) infection in the skeletal muscle of carp, Cyprinus carpio L. Journal of Fish Biology 41: 363–371. https://doi.org/10.1111/j.1095-8649.1992.tb02665.x
Patra S., Sojková P., Peckova H., Fiala I., Eszterbauer E. & Holzer A. 2018. Biodiversity and host-parasite cophylogeny of Sphaerospora (sensu stricto) (Cnidaria: Myxozoa). Parasites and Vectors 11 (1): e347. https://doi.org/10.1186/s13071-018-2863-z
Press C.M. 1998. Immunology of fishes. In: Pastoret P.P, Griegel P., Bazin H. & Govaerts A. (eds) Handbook of Vertebrate Immunology: 3–62. Academic Press, San Diego.
Reed C.C., Basson L. & Van As L.L. 2003. Myxozoans infecting the sharptooth catfish, Clarias gariepinus in the Okavango River and Delta, Botswana, including descriptions of two new species, Henneguya samochimensis sp. n. and Myxobolus gariepinus sp. n. Folia Parasitologica (Praha) 50 (3): 183–189. https://doi.org/10.14411/fp.2003.033
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029
Sakiti G.N. 1997. Myxosporidia and Microsporidia Fish Parasites in Southern Benin: Faunal Description, Ultrastructure and Biology. PhD thesis. National University of Benin.
Stiassny M.L.G., Teugels G.G. & Hopkins C.D. 2007. Freshwater and brackish fish from Lower Guinea, western Central Africa. In: IRD (ed.) Tropical Fauna and Flora Collection, 1. IRD, Paris.
Zhang J.Y., Gu Z.M., Kalavati C., Costa Eiras J., Liu Y., Guo Q.Y. & Molnár K. 2013. Synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Systematic Parasitology 86 (3): 235–256. https://doi.org/10.1007/s11230-013-9449-0
Zhang J.Y., Al-Quraishy S. & Abdel-Baki A.A. 2014. The morphological and molecular characterization of Myxobolus khaliji n. sp. (Myxozoa: Myxosporea) from the double bar seabream Acanthopagrus bifasciatus (Forsskal, 1775) in the Arabian Gulf, Saudi Arabia. Parasitology Research 113 (6): 2177– 2183. https://doi.org/10.1007/s00436-014-3870-4
Zhao Y., Liu X., Xi B., Zhang Q., Li A. & Zhang J. 2020. Transcriptomic analysis of oligochaete immune responses to myxosporeans infection: Branchiura sowerbyi infected with Myxobolus cultus. Journal of Invertebrate Pathology 169: e107283. https://doi.org/10.1016/j.jip.2019.107283
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