Abstract
Members of the myxozoan genus Kudoa (Myxosporea: Multivalvulida: Kudoidae) are characterized as having four or more shell valves in a myxospore, with a corresponding number of polar capsules. Certain Kudoa spp. are critical pathogens in fish, causing postmortem myoliquefaction, unmarketable fish musculature due to unsightly macroscopic cysts, and reduced aquaculture production due to the outbreaks of neurological symptoms or cardiac diseases. Molecular genetic techniques have enabled the differentiation of Kudoa spp. with morphologically similar myxospores. In the present study, we employed integrated taxonomic approaches on five Kudoa spp. forming cysts between the trunk muscle myofibers (K. bora from Osteomugil perusii and K. lutjanus from Acanthopagrus latus), or cysts in the gallbladder wall (K. petala from Sillago sihama), and pseudocysts in the trunk muscle myofibers (K. uncinata from Nuchequula nuchalis and K. fujitai n. sp. from O. perusii). These four host fishes, which originated in the South China Sea, were purchased in the wet markets in Zhanjiang City, Guangdong Province, China, between August 2016 and April 2018. We have redescribed the four Kudoa spp. (K. bora, K. lutjanus, K. petala, and K. uncinata) on which little data are available after their original descriptions. Particularly, genetic characterization of K. bora and K. lutjanus, which are known to have myxospores morphologically similar to those of K. iwatai, was performed based on the nuclear ribosomal RNA gene and partial mitochondrial DNA genes such as cytochrome c oxidase subunit I and small and large ribosomal genes, demonstrating the validity and independence of these three kudoid species. We also provide description of a new species—K. fujitai n. sp.—in the present study. Application of integrated taxonomic approaches to known species characterized solely based on morphological criteria, as well as unknown species (e.g., K. fujitai n. sp. in the present study), contributes to better understanding of the biodiversity of Kudoa and multivalvulid myxosporeans.
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References
Abdel-Baki AS, Abdel-Haleem HM, Al-Quraishy S, Azevedo C, Mansour L (2018) Ultrastructural and molecular characteristics of Kudoa crenimugilis n. sp. infecting intestinal smooth muscle of fringelip mullet Creninmugil crenilabis in the Red Sea. Dis Aquati Organ 129:53–62
Akaishi F, Easy R, St-Jean S, Courtenay S, Ribeiro CA, Cone D (2004) Supplemental diagnosis of Kudoa funduli (Myxozoa) parasitizing Fundulus heteroclitus (Cyprinodontidae) from coastal northeastern North America. J Parasitol 90:477–480
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, Cham, pp 111–123
Burger MAA, Adlard RD (2010) 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, 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
Casal G, Soares EC, Rocha S, Silva TJ, Santos EL, Nascimento R, Oliveira E, Zaevedo C (2019) Description of a new myxozoan Kudoa eugerres n. sp. and reclassification of two Sphaerospora sensu lato species. Parasitol Res 118:1719–1730
Chen C, Ma C (1998) Fauna Sinica. Myxozoa, Myxosporea. Science Press, Beijing, p 806 with 180 figure plates (in Chinese)
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
Diamant A, Ucko M, Paperna I, Colorni A, Lipshitz A (2005) Kudoa iwatai (Myxosporea: Multivalvulida) in wild and cultured fish in the Red Sea: Redescription and molecular phylogeny. J Parasitol 91:1175–1189
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 Jpn Soc Sci Fish 46:1193–1198
Egusa S, Shiomitsu T (1983) Two new species of the genus Kudoa (Myxosporea: Multivalvulida) from marine cultured fishes in Japan. Fish Pathol 18:163–171 (in Japanese with English summary)
Eiras JC, Saraiva A, Cruz C (2014) Synopsis of the species of Kudoa Meglitsch, 1947 (Myxozoa: Myxosporea: Multivalvulida). Syst Parasitol 87:153–180
Fiala I, Bartošová-Sojková P, Whipps CM (2015) Classification and phylogenetics of Myxozoa. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing Switzerland, Cham, pp 85–110
Fujita T (1930) On a new Myxosporidia in the muscle of the gray-mullet Chloromyxum bora nov. sp. Zool Mag (Tokyo) 42:45–48 (in Japanese with English summary)
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hervio DML, Khattra J, Devlin RH, Kent ML, Sakanari J, Yokoyama H (1997) Taxonomy of Kudoa species (Myxosporea), using a small-subunit ribosomal DNA sequence. Can J Zool 75:2112–2119
Joy JE (1972) A new species of Kudoa (Myxosporidea: Chloromyxidae) from the spot, Leiostomus xanthurus Lacépède, in Clear Lake, Texas. J Protozool 19:264–265
Kalavati C, Nandi NC (2007) Handbook on Myxosporean parasites of Indian fishes. Zoological Survey of India, Kolkata, p 293 with 5 figure plates
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
Kawai T, Sekizuka T, Yahata Y, Kuroda M, Kumeda Y, Iijima Y, Kamata Y, Sugita-Konishi Y, 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. Clin Infect Dis 54:1046–1052
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 (2020) Phylogenetic characterization of seven Unicapsula spp. (Myxozoa: Myxosporea: Multivalvulida) from commercial fish in southern China and Japan. Parasitology. https://doi.org/10.1017/S0031182019001793
Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156
Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36
Lom J, Dyková I, Lhotáková Š (1983) Kudoa lunata n. sp. (Myxozoa, Myxosporea) and notes on the nature of muscular “cysts” of the genus Kudoa. Arch Protistenkd 127:387–397
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
Matsukane Y, Sato H, Tanaka S, Kamata Y, Sugita-Konishi S (2011) Kudoa iwatai and two novel Kudoa spp., K. trachuri n. sp. and K. thunni n. sp. (Myxosporea: Multivalvulida), from daily consumed marine fish in western Japan. Parasitol Res 108:913–926
Meglitsch PA (1947) Studies on Myxosporidia from the Beaufort region. II. Observations on Kudoa clupeidae (Hahn) gen. nov. J Parasitol 33(33):271–277
Moran JDW, Whitaker DJ, Kent ML (1999) A review of the myxosporean genus Kudoa Meglitsh, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172:163–196
Ohnishi T, Obara T, Arai S, Yoshinari T, Sugita-Konishi Y (2018) Quantitative analysis of Unicapsula seriolae in greater amberjack associated with unidentified food-borne disease. Food Hyg Safe Sci 59:24–29
Özer A, Okkay S, Gürkanli CT, Çiftçi Y, Yurankhno V (2018) Two novel myxosporean parasites in Black Sea fishes: Kudoa niluferi sp. nov. and Kudoa anatolica sp. nov. (Cnidaria: Myxospoea). Dis Aquat Org 128:225–233
Reimschuessel R, Gieseker CM, Driscoll C, Baya A, Kane AS, Blazer VS, Evans JJ, Kent ML, Moran JDW, Poynton SL (2003) Myxosporean plasmodial infection associated with ulcerative lesions in young-of-the-year Atlantic menhaden in a tributary of the Chesapeake Bay, and possible links to Kudoa clupeidae. Dis Aquat Org 53:143–166
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
Sarkar NK, Ghosh S (1991) Two new coelozoic myxosporida (Myxozoa: Myxosporea) from estuarine teleost fishes (Mugilidae) of West Bengal, India. Proc Zool Soc Calcutta 44:131–135. (Cited in Kalavati and Nandi 2007)
Sarkar NK, Mazumdar S (1983) Studies on myxosporidian parasites (Myxozoa: Myxosomatidae) from marine fishes in West Bengal, India. I. Description of three new species from Tachysurus sp. Archiv für Protistenkunde 127(1):59–63. (Cited in Kalavati and Nandi 2007)
Sato H, Kasai A (2016) Kudoa species (Myxozoa: Myxosporea: Multivalvulida) recorded in Japan or its surrounding natural waters (1930–2016). Jpn J Vet Parasitol 15:111–138 (in Japanese with English summary)
Shin SP, Shirakashi S, Hamano S, Kato K, Lasso LT, Yokoyama H (2016) Phylogenetic study of the genus Kudoa (Myxozoa: Multivalvulida) with a description of Kudoa rayformis sp. nov. from the trunk muscle of Pacific sierra Scomberomorus sierra. Mol Phylogenet Evol 98:337–345
Shul’man SS (1966) Myxosporidia of the USSR. Nauka Publishers (English book translated from Russian, New Delhi, India: Amerind Publishing in 1988), Moscow, p 643
Sugita-Konishi Y, Sato H, Ohnishi T (2014) Novel foodborne disease associated with consumption of raw fish, olive flounder (Paralichthys olivaceus). Food Safe 2:141–150
Suzuki J, Murata R, Yokoyama H, Sadamasu K, Kai A (2015) Detection rate of diarrhea-causing Kudoa hexapunctata in pacific Bluefin tuna Thunnus orientalis from Japanese waters. Int J Food Microbiol 194:1–6
Takeuchi F, Sekizuka T, Ogasawara Y, Yokoyama H, Kamikawa R, Inagaki Y, Nozaki T, Sugita-Konishi Y, Ohnishi T, Kuroda M (2015) The mitochondrial genomes of a myxozoan genus Kudoa are extremely divergent in Metazoa. PLoS One 10:e0132030
Thompson JD, Higgins DG, 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 Res 22:4673–4680
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115
Velasco M, Neto JLS, Videira M, do Nascimento LCS, Gonçalves EC, Matos E (2019) Kudoa amazonica n. sp. (Myxozoa; Multivalvulida), a parasite of the esophageal musculature of the freshwater catfish, Hypophthalmus marginatus (Siluriformes: Pimelodidae), from a river of the Amazon region. Microb Pathog 130:247–252
Wang PC, Huang JP, Tsai MA, Cheng SY, Tsai SS, Chen SD, Chen SP, Chu SH, Liaw LL, Chang LT, Chen SC (2005) Systemic infection of Kudoa lutjanus n. sp. (Myxo-zoa: Myxosporea) in red snapper Lutjanus erythropterus from Taiwan. Dis Aquat Org 67:115–124
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert DN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc B (Biol Sci) 360:1847–1857
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, Kent ML (2003) Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Myltivalvulida) from the muscle of Spanish mackerel (Scomberomorus commerson) from the Great Barrier Reef, Australia. J Parasitol 89:168–173
Whipps CM, Grossel G, Adlard RD, Yokoyama H, Bryant MS, Munday BL, Kent ML (2004) Phylogeny of the Multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. J Parasitol 90:618–622
Whitaker DJ, Kent ML, Sakanari JA (1996) Kudoa minauriculata n. sp. (Myxozoa, Myxosporea) from the musculature of bocaccio (Sebastes paucispinis) from California. J Parasitol 82:312–315
Xie XR, Chen QL (1988) A new genus and species of family Tetracapsulidae from marine fishes in South China Sea (Myxosporea: Multivalvulida). Oceanologia et Limnologia Sinica 19:431–434
Yasunaga N, Hatai K, Ogawa S, Yasumoto S (1981) An unknown myxozoa found in brain of cultured sea bass, Lateolabrax japonicus and cultured Japanese striped knifejaw, Oplegnathus fasciatus. Fish Pathol 16:51–54
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
Zhang JB, Hanner R (2011) DNA barcoding is a useful tool for the identification of marine fishes from Japan. Biochem Syst Ecol 39:31–42
Zhou Y, Zhao Y-J (2008) Description of three new species of Kudoa (Myxosporea, Multivalvulida, Kudoiae) parasitic in marine fishes from the East China Sea. Acta Hydrobiol Sinica 32(Suppl):51–56 (in Chinese with English summary)
Acknowledgements
We are indebted to Prof. Hiroyuki Motomura (Kagoshima University Museum) for his assistance in the taxonomic identification of the host fish species and Prof. Emeritus Shuhei Tanaka (Faculty of Agriculture, Yamaguchi University) for his help with the scanning electron microscopy of Kudoa myxospores (not shown in the present study).
Funding
This study was partially supported by a Grant-in-Aid for Young Ph.D. Researcher (No: R17022) from the Faculty of Agricultural Science, Guangdong Ocean University (YCL), Grant-in-Aid for Food Science and Research 2017 from The Towa Foundation (HS), Grant-in-Aid for Food Science and Research 2019 from The Toyo Suisan Foundation (HS), Grant-in-Aid for International Collaboration Research 2019 from the Goho life Sciences International Fund (JYZ), and JSPS KAKENHI grant number 18 K05995 (HS). Special thanks are extended to the United Graduate School of Veterinary Science, Yamaguchi University, and Institute of Hydrobiology, Chinese Academy of Science, for supporting international collaborative research (travel grants for YCL and JYZ, respectively).
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Li, YC., Inoue, K., Zhang, JY. et al. 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 (2020). https://doi.org/10.1007/s00436-020-06636-0
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DOI: https://doi.org/10.1007/s00436-020-06636-0