Abstract
Multiple Kudoa spp. (Myxozoa: Myxosporea: Multivalvulida) have been recorded in Japanese parrotfish (Calotomus japonicus) from the Philippine Sea (Northwest Pacific Ocean), off southwestern Japan; Kudoa yasunagai in the brain, and K. igami, K. lateolabracis, and K. thalassomi in the muscles. This study examined eight Philippine Sea Japanese parrotfish samples collected in January and February 2019 and found K. prunusi in the brain (3–57 plasmodia/fish; average 17.9) and K. lateolabracis plasmodia in the trunk muscle of all fish individuals examined. The K. prunusi in this study was characterized by myxospores predominatetly with six shell valves (SVs) and a corresponding number of polar capsules (PCs), contrasting with the original description of the species from farmed Pacific bluefin tuna (Thunnus orientalis) brain that characterized the species as having predominately five SVs/PCs. Molecular-genetic characterization of 18S and 28S ribosomal RNA genes and mitochondrial DNA genes (cytochrome c oxidase subunit 1 and small and large ribosomal RNA subunits) clearly differentiated the K. prunusi isolate from K. yasunagai, commonly characterized by six or seven, but rarely five, SVs/PCs myxospores. The Japanese parrotfish is a new host record for K. prunusi and speculated to be an important reservoir host in its natural waters. Kudoa lateolabracis myxospores isolated from pseudocysts in the myofiber were morphologically and phylogenetically close to a clade of the Kudoa spp. that exhibit cruciform myxospores similar to K. thyrsites. This study is the first to sequence a mitochondrial DNA of small and large subunit ribosomal RNA of K. lateolabracis.
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References
Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552
Atkinson SD, Bartošová-Sojková P, Whipps CM, Bartholomew JL (2015) Approaches for characterising myxozoan species. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Switzerland, pp 111–123
Burger MAA, Adlard RD (2010a) Four new species of Kudoa Meglitsch, 1947 (Myxosporea: Multivalvulida) from Australia with recommendations for species descriptions in the Kudoidae. Parasitology 137:793–814
Burger MAA, Adlard RD (2010b) Phenotypic variation in a significant spore character in Kudoa (Myxosporea: Multivalvulida) species infecting brain tissue. Parasitology 137:1759–1772
Burger MAA, Adlard RD (2011) Low host specificity in the Kudoidae (Myxosporea: Multivalvulida) including seventeen new host records for Kudoa thalassomi. Folia Parasitol 58:1–16
Burger MAA, Cribb TH, Adlard RD (2007) Patterns of relatedness in the Kudoidae with descriptions of Kudoa chaetodoni n. sp. and K lethrini n. sp. (Myxosporea: Multivalvulida). Parasitology 134:669–681
Burger MAA, Barnes AC, Adlard RD (2008) Wildlife as reservoirs for parasites infecting commercial species: host specificity and a redescription of Kudoa amamiensis from teleost fish in Australia. J Fish Dis 31:835–844
Dawson-Coates JA, Chase JC, Funk V, Booy MH, Haines LR, Falkenberg CL, Whitaker DJ, Olafson RW, Pearson TW (2003) The relationship between flesh quality and numbers of Kudoa thyrsites plasmodia and spores in farmed Atlantic salmon, Salmo salar L. J Fish Dis 26:451–459
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469
Egusa S (1986) The order Multivalvulida Shulman, 1959 (Myxozoa: Myxosporea): a review. Fish Pathol 21:261–274 ((in Japanese with English summary))
Egusa S, Nakajima K (1980) Kudoa amamiensis n. sp. (Myxosporea: Multivalvulida) found in cultured yellowtails and wild damselfishes from Amami-Ohshima and Okinawa, Japan. Bull Japan Soc Sci Fish 46:1193–1198
Funk VA, Raap M, Sojonky K, Jones S, Robinson J, Falkenberg C, Miller KM (2007) Development and validation of an RNA- and DNA-based quantitative PCR assay for determination of Kudoa thyrsites infection levels in Atlantic salmon Salmo salar. Dis Aquat Org 75:239–249
Funk VA, Olafson RW, Raap M, Smith D, Aitken L, Haddow JD, Wang D, Dawson-Coates JA, Burke RD, Miller KM (2008) Identification, characterization and deduced amino acid sequence of the dominant protease from Kudoa paniformis and K. thyrsites; a unique cytoplasmic cysterine protease. Comp Biochem Physiol B 149:477–489
Giulietti L, Karlsbakk E, Cipriani P, Shayo SD, Storesund JE, Levsen A (2020) Molecular characterization of the myoliquefactive fish parasite Kudoa mirabilis (Cnidaria, Kudoidae) from SW Indian Ocean and its phylogenetic relationship with the Kudoa thyrsites species complex. Microorganisms 8:1352. https://doi.org/10.3390/microorganisms8091352
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Heiniger H, Cribb TH, Adlard RD (2013) Intra-specific variation of Kudoa spp. (Myxosporea: Multivalvulida) from apogonid fishes (Perciformes), including the description of two new species, K. cheilodipteri n. sp. and K. cookii n. sp., from Australian waters. Syst Parasitol 84:193–215
Inoue K, Li Y-C, Ghosh S, Yunus M, Zhang J-Y, Sato H (2021) Identification of a new species, Unicapsula aequilobata n. sp., and Unicapsula seriolae (Myxozoa: Myxosporea: Multivalvulida) in carangid fish from the South China Sea. Parasitol Res 120:2379–2389
Kabata Z, Whitaker DJ (1981) Two species of Kudoa (Myxosporea: Multivalvulida) parasitic in the flesh of Merluccius productus (Ayres, 1855) (Pisces: Teleostei) in the Canadian Pacific. Can J Zool 59:2085–2091
Kasai A, Li Y-C, Setsuda A, Mafie E, Sato H (2015) Genetic characterization of Kudoa iwatai and Kudoa trachuri in commercial marine fish (Platycephalus sp. and Trachurus japonicus) for human consumption. Jpn J Vet Parasitol 14:22–30
Kasai A, Li Y-C, Mafie E, Sato H (2016a) Morphological and molecular genetic characterization of two Kudoa spp., K. musculoliquefaciens, and K. pleurogrammi n. sp. (Myxosporea: Multivalvulida), causing myoliquefaction of commercial marine fish. Parasitol Res 115:1883–1892
Kasai A, Li Y-C, Mafie E, Sato H (2016b) 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). Parasitol Res 115:2741–2755
Kasai A, Setsuda A, Sato H (2017a) Morphological and genetic characterization of Kudoa whippsi (Myxosporea: Multivalvulida) from Cheilodactylus zonatus in the western Pacific Ocean off Japan, and two new Kudoa spp. (K. akihitoi n. sp. and K. empressmichikoae n. sp.) from Acanthogobius hasta in the Sea of Ariake. Japan Parasitol Res 116:647–659
Kasai A, Tsuduki H, Jimenez LA, Li Y-C, Tanaka S, Sato H (2017b) Incidence of three Kudoa spp., K. neothunni, K. hexapunctata, and K. thunni (Myxosporea: Multivalvulida), in Thunnus tunas distributed in the western Pacific Ocean. Parasitol Res 116:1137–1150
Konagaya S (1984) Studies on the jellied meat of fish, with special reference to that of yellowfin tuna. Bull Tokai Reg Fish Res Lab 114:1–101 ((in Japanese with English summary))
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lester RJG (1982) Unicapsula seriolae n. sp. (Myxosporea, Multivalvulida) from Australian yellowtail Kingfish Seriola lalandi. J Protozool 29:584–587
Li Y-C, Sato H, Tanaka S, Ohnishi T, Kamata Y, 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). Parasitol Res 112:1991–2003
Li Y-C, Tamemasa S, Zhang J-Y, Sato H (2020a) Phylogenetic relationships of three Kudoa spp. with morphologically similar myxospores (K. iwatai, K. lutjanus, and K. bora), with the redescription of K. uncinata and K. petala and description of a new species (K. fujitai n. sp.) in fishes in the South China Sea. Parasitol Res 119:1221–1236
Li Y-C, Inoue K, Tanaka S, Zhang J-Y, Sato H (2020b) Identification of four new Kudoa spp. (Myxozoa: Myxosporea: Multivalvulida) in commercial fishes collected from South China Sea, Atlantic Ocean, and Bering Sea by integrated taxonomic approach. Parasitol Res 119:2113–2128
Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156
Matsukane Y, Sato H, Tanaka S, Kamata Y, Sugita-Konishi Y (2010) Kudoa septempunctata n. sp. (Myxosporea: Multivalvulida) from an aquacultured olive flounder (Paralichthys olivaceus) imported from Korea. Parasitol Res 107:865–872
Matsumoto K (1954) On the two new Myxospridia, Chloromyxum musculoliquefaciens sp. nov. and Neochloromyxum cruciformum gen. et sp. nov., from the jellied muscle of swordfish, Xiphias glandius Linné, and Lateolabrax japonicus (Temmink et Schlegel). Bull Japan Soc Sci Fish 20:469–478
Meng F, Yokoyama H, Shirakashi S, Grabner D, Ogawa K, Ishimaru K, Sawada Y, Murata O (2011) Kudoa prunusi n. sp. (Myxozoa: Myxosporea) from the brain of Pacific bluefin tuna Thunnus orientalis (Temminck & Schlegel, 1844) cultured in Japan. Parasitol Int 60:90–96
Miller TL, Adlard RD (2012) Brain infecting kudoids of Australia’s coral reefs, including a description of Kudoa lemniscati n. sp. (Myxosporea: Kudoidae) from Lutjanus lemniscatus (Perciformes: Lutjanidae) off Ningaloo Reef, Western Australia. Parasitol Int 61:333–342
Moran JDW, Whitaker DJ, Kent ML (1999) A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172:163–196
Sakai H, Kato E, Sakaguchi S, Setsuda A, Sato H (2018) Morphological and molecular genetic characterization of Kudoa konishiae n. sp. (Myxosporea: Multivalvulida) in the muscle of Japanese Spanish mackerel (Scomberomorus niphonius). Parasitol Res 117:893–904
Sakai H, Kawai T, Zhang J, Sato H (2019) New host records of three Kudoa spp. (K. yasunagai, K. thalassomi, and K. igami) with notable variation in the number of shell valves and polar capsules in spores. Parasitol Res 118:143–157
Shin SP, Ishitani H, Shirakashi S (2016) Development of a multiplex PCR to detect Kudoa spp. and to distinguish Kudoa septempunctata in olive flounder Paralichthys olivaceus. Aquaculture 464:37–41
Shirakashi S, Yamane IH, Yanagida T, Yokoyama H (2014) First report of Kudoa species in the somatic muscle of the Japanese parrotfish Calotomus japonicus (Scaridae) and a description of Kudoa igami, n. sp. (Myxozoa: Multivalvulida). Parasitol Res 113:2515–2524
Sugiyama A, Yokoyama H, Ogawa K (1999) Epizootiological investigation on kudoosis amami caused by Kudoa amamiensis (Multivalvulida: Myxozoa) in Okinawa Prefecture, Japan. Fish Pathol 34:39–43 ((in Japanese with English summary))
Takeuchi F, Ogasawara Y, Kato K, Sekizuka T, Nozaki T, Sugita-Konishi Y, Ohnishi T, Kuroda M (2016) Genetic variants of Kudoa septempunctata (Myxozoa: Multivalvulida), a flounder parasite causing foodborne disease. J Fish Dis 39:667–672
Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53:364–373
Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlay V, Kent ML (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). J Eukaryot Microbiol 50:215–219
Yokoyama H, Itoh N (2005) Two multivalvulid myxozoans causing postmortem myoliquefaction: Kudoa megacapsula n. sp. from red barracuda (Sphyraena pinguis) and Kudoa thyrsites from splendid alfonso (Beryx splendens). J Parasitol 91:1132–1137
Yokoyama H, Whipps CM, Kent ML, Mizuno K, Kawakami H (2004) Kudoa thyrsites from Japanese flounder and Kudoa lateolabracis n. sp. from Chinese Sea bass: causative myxozoans of post-mortem myoliquefaction. Fish Pathol 39:79–85
Yokoyama H, Yanagida T, Takemaru I (2006) The first record of Kudoa megacapsula (Myxozoa: Multivalvulida) from farmed yellowtail Seriola quinqueradiata originating from wild seedlings in south Korea. Fish Pathol 41:159–163
Yokoyama H, Mekata T, Satoh J, Nishioka T, Mori K (2017) Morphological and molecular comparisons between Japanese and Korean Isolates of Kudoa septempunctata (Myxozoa: Multivalvulida) in the olive flounder Paralichthys olivaceus. Fish Pathol 52:152–157
Zhou LS, Li-Chan ECY (2009) Effect of Kudoa spores, endogenous protease activity and frozen storage on cooked texture of minced Pacific hake (Merluccius productus). Food Chem 11:1076–1082
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This study was partially supported by a Grant-in-Aid for Food Science and Research 2019 from The Toyo Suisan Foundation (HS) and the Japan Society for the Promotion of Science (JSPS) KAKENHI grant number 18K05995 (HS).
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Inoue, K., Kasai, A., Rosyadi, I. et al. Occurrence of Kudoa prunusi and K. lateolabracis (Myxozoa: Myxosporea: Multivalvulida) in Philippine-Sea Japanese parrotfish (Calotomus japonicus). Parasitol Res 121, 601–612 (2022). https://doi.org/10.1007/s00436-021-07418-y
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DOI: https://doi.org/10.1007/s00436-021-07418-y