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Phylogenetic characterisation of seven Unicapsula spp. (Myxozoa: Myxosporea: Multivalvulida) from commercial fish in southern China and Japan

Published online by Cambridge University Press:  26 December 2019

Ying-Chun Li ,
Souhei Tamemasa ,
Jin-Yong Zhang Open the ORCID record for Jin-Yong Zhang [Opens in a new window]  and
Hiroshi Sato Open the ORCID record for Hiroshi Sato [Opens in a new window]
Ying-Chun Li
Affiliation:
Faculty of Agricultural Science, Guangdong Ocean University, Mazhang, Zhanjiang, Guangdong524088, China
Souhei Tamemasa
Affiliation:
Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, 1677-1 Yoshida, Yamaguchi753-8515, Japan
Jin-Yong Zhang
Affiliation:
Fish Diseases Laboratory, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan430072, China
Hiroshi Sato*
Affiliation:
Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, 1677-1 Yoshida, Yamaguchi753-8515, Japan
*
Author for correspondence: Hiroshi Sato, E-mail: sato7dp4@yamaguchi-u.ac.jp
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Abstract

The myxozoan genus Unicapsula Davis, 1924 (Myxosporea: Multivalvulida: Trilosporidae) is characterized as having one functional polar capsule (PC) and two rudimentary PCs in a three-valved myxospore. The plasmodia of Unicapsula spp. grow either in the myofibres or in the gills, oesophageal walls and urinary organs of marine fish. Few studies have investigated the taxonomy of Unicapsula spp. including the type species Unicapsula muscularis. Accordingly, the taxonomy of the genus was explored in the present study by using 15 new isolates of seven Unicapsula spp. (U. muscularis, U. galeata, U. andersenae, U. pyramidata, U. pflugfelderi, and two new species) that had formed pseudocysts in the trunk myofibres of commercial fish collected in southern China and Japan from November 2015 to January 2019. Two new species Unicapsula trigona n. sp., and Unicapsula motomurai n. sp. exhibited unique myxospore morphologies (semi-triangular and spherical myxospores, respectively) and 18S and 28S rDNA sequences that were distinct from those of the other Unicapsula spp. Phylogenetic analysis of the 18S and 28S rDNA sequences confirmed the monophyletic status of Unicapsula.

Keywords

Integrated taxonomyMyxozoanew host recordrDNAUnicapsula motomurai n. sp.Unicapsula trigona n. sp.Unicapsula
Type
Research Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 448 - 464
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Copyright
Copyright © Cambridge University Press 2019

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References

Alama-Bermejo, G, Cuadrado, M, Raga, JA and Holzer, AS (2009) Morphological and molecular redescription of the myxozoan Unicapsula Pflugfelderi Schubert, Sprague & Reinboth 1975 from two teleost hosts in the Mediterranean. A review of the genus Unicapsula Davis 1924. Journal of Fish Diseases 32, 335–350.CrossRefGoogle ScholarPubMed
Al-Jufaili, SH, Freeman, MA, Machkevskyi, VK, Al-Nabhani, A and Palm, HW (2016) Morphological, ultrastructural, and molecular description of Unicapsula fatimae n. sp. (Myxosporea: Trilosporidae) of whitespotted rabbitfish (Siganus canaliculatus) in Omani waters. Parasitology Research 115, 1173–1184.CrossRefGoogle ScholarPubMed
Anisimova, M and Gascuel, O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539–552.CrossRefGoogle ScholarPubMed
Aseeva, NL and Krasin, VK (2001) On new records of the family Trilosporidae (Myxosporida: Multivalvulida) from fishes of Pacific Ocean. Parazitologiya 35, 353–356.Google Scholar
Burger, MAA and Adlard, RD (2011) Low host specificity in the Kudoidae (Myxosporea: Multivalvulida) including seventeen new host records for Kudoa thalassomi. Folia Parasitologica 58, 1–16.CrossRefGoogle ScholarPubMed
Davis, HS (1924) A new myxosporidian parasite, the cause of “wormy” halibut. Report of the U. S. Commercial Fisheries for 1923 Appendix 8, 1–5.Google Scholar
Dereeper, A, Guignon, V, Blanc, G, Audic, S, Buffet, S, Chevenet, F, Dufayard, JF, Guindon, S, Lefort, V, Lescot, M, Claverie, J-M and Gascuel, O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, 465–469.CrossRefGoogle ScholarPubMed
Diebakate, C, Fall, M, Faye, N and Toguebaye, BS (1999) Unicapsula marquesi n. sp. (Myxosporea, Multivalvulida) parasite des branchies de Polydactylus Quadrifilis (Cuvier, 1829) (Poisson, Polynemidae) des côtes sénégalaises (Afrique de l'Ouest). Parasite 6, 231–235.CrossRefGoogle Scholar
Fiala, I, Bartošová-Sojková, P and Whipps, CM (2015) Classification and phylogenetics of Myxozoa. In Okamura, B, Gruhl, A and Bartholomew, JL (eds), Myxozoan Evolution, Ecology and Development. Cham, Switzerland: Springer International Publishing AG, pp. 85–110.CrossRefGoogle Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Kasai, A, Li, Y-C, Mafie, E and Sato, H (2016) New host records of monacanthid fish for three Kudoa spp. (K. septempunctata, K. thyrsites, and K. shiomitsui) prevalent in the olive flounder (Paralichthys olivaceus), with the description of K. parathyrsites n. sp. from a black scraper (Thamnaconus modestus). Parasitology Research 115, 2741–2755.CrossRefGoogle Scholar
Kawai, T, Sekizuka, T, Yahata, Y, Kuroda, M, Kumeda, Y, Iijima, Y, Kamata, Y, Sugita-Konishi, Y and Ohnishi, T (2012) Identification of Kudoa septempunctata as the causative agent of novel food poisoning outbreaks in Japan by consumption of Paralichthys olivaceus in raw fish. Clinical Infectious Diseases 54, 1046–1052.CrossRefGoogle ScholarPubMed
Lester, RJG (1982) Unicapsula seriolae n. sp. (Myxosporea, Multivalvulida) from Australian yellowtail kingfish Seriola lalandi. Journal of Protozoology 29, 584–587.CrossRefGoogle Scholar
Li, Y-C, Sato, H, Tanaka, S, Ohnishi, T, Kamata, Y and Sugita-Konishi, Y (2013) Characterization of the ribosomal RNA gene of Kudoa neothunni (Myxosporea: Multivalvulida) in tunas (Thunnus spp.) and Kudoa scomberi n. sp. in a chub mackerel (Scomber japonicus). Parasitology Research 112, 1991–2003.CrossRefGoogle Scholar
Lom, J and Noble, ER (1984) Revised classification of the class Myxosporea Bütschli, 1881. Folia Parasitologica 31, 193–205.Google Scholar
Lom, J and Arthur, JR (1989) A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151–156.CrossRefGoogle Scholar
Lom, J and Dyková, I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.CrossRefGoogle ScholarPubMed
Miller, TL and Adlard, RD (2013) Unicapsula species (Myxosporea: Trilosporidae) of Australian marine fishes, including the description of Unicapsula andersenae n. sp. in five teleost families off Queensland, Australia. Parasitology Research 112, 2945–2957.CrossRefGoogle ScholarPubMed
Motomura, H (2004) Theadfins of the World (Family Polynemidae). An annotated and illustrated catalogue of polynemid species known to date. FAO Species Catalogue for Fishery Purposes. No. 3.Google Scholar
Naidjenova, NN and Zaika, VE (1970) Three new genera of myxosporean parasites of fish from the Indian Ocean. Zoological Zhournal 49, 451–454, (in Russian with English summary).Google Scholar
Nakada, M (2008) Capture-based aquaculture of yellowtail. In Lovatelli, A and Holthus, PF (eds), Capture-based Aquaculture: Global Overview. Roma, Italy: FAO, Fisheries Technical Paper, No. 508, pp. 199–215.Google Scholar
Ohnishi, T, Obara, T, Arai, S, Yoshinari, T and Sugita-Konishi, Y (2018) Quantitative analysis of Unicapsula seriolae in greater amberjack associated with unidentified food-borne disease. Food Hygiene and Safety Science 59, 24–29, (in Japanese with English summary).CrossRefGoogle ScholarPubMed
Sarkar, NK (1984) A species of Unicapsula Davis, 1924 (Myxozoa) infecting a fish of the southern coast of India. International Journal of Academy of Ichthyology, Modinagar 5, 187–189.Google Scholar
Sarkar, NK (1999) Some new Myxosporidia (Myxozoa: Myxosporea) of the genera Myxobolus Butschli, 1882 Unicapsula Davis, 1942 Kudoa Meglitsch, 1947 Ortholinea Shulman, 1962 and Neoparvicapsula Gaevskaya, Kovaleva and Shulman, 1982. Proceedings of the Zoological Society Calcutta 52, 38–48.Google Scholar
Schubert, G, Sprague, V and Reinboth, R (1975) Observations on a new species of Unicapsula (Myxosporida) in the fish Maena Smaris (L.) by conventional and electronmicroscopy. Zeitschrift für Parasitenkunde 46, 245–252.CrossRefGoogle Scholar
Sugita-Konishi, Y, Sato, H and Ohnishi, T (2014) Novel foodborne disease associated with consumption of raw fish, olive flounder (Paralichthys olivaceus). Food Safety 2, 141–150.CrossRefGoogle Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Tomochi, H, Li, Y-C, Tran, BT, Yanagida, T and Sato, H (2014) Three Unicapsula species (Myxosporea: Trilosporidae) of Asian marine fishes, including the description of Unicapsula setoensis n. sp. in the yellowfin goby (Acanthogobius flavimanus) from the Inland Sea of Japan. Parasitology Research 113, 3807–3816.CrossRefGoogle ScholarPubMed
Ward, RD, Zemlak, TS, Innes, BH, Last, PR and Hebert, DN (2005) DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society. B, Biological Sciences 360, 1847–1857.CrossRefGoogle ScholarPubMed
Whipps, CM and Kent, ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). Journal of Eukaryotic Microbiology 53, 364–373.CrossRefGoogle Scholar
Whipps, CM, Grossel, G, Adlard, RD, Yokoyama, H, Bryant, MS, Munday, BL and Kent, ML (2004) Phylogeny of the Multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. Journal of Parasitology 90, 618–622.CrossRefGoogle ScholarPubMed
Yokoyama, H, Abe, N, Maehara, T and Suzuki, J (2014) First record of Unicapsula seriolae (Myxozoa: Multivalvulida) from the muscle of Malabar grouper Epinephelus malabaricus in Japan. Parasitology International 63, 561–566.CrossRefGoogle ScholarPubMed
Zhang, JB and Hanner, R (2011) DNA barcoding is a useful tool for the identification of marine fishes from Japan. Biochemical Systematics and Ecology 39, 31–42.CrossRefGoogle Scholar