Abstract
Myxosporean genera Henneguya and Myxobolus (Bivalvulida: Myxobolidae) are closely related in morphology and molecular phylogeny, speciose with approximately 1,000 nominal species. The majority of them are recorded from freshwater fish worldwide, and few are known from marine fish. In this study, three myxobolid spp. are described from marine fish around Japan. Two novel Henneguya spp., Henneguya ogawai sp. n. and Henneguya yokoyamai sp. n., are described from two black sea breams (Acanthopagrus schlegelii) fished in the Inland Sea (Setonaikai), Japan. Plasmodia of the former species were localized in the esophageal or intestinal wall, and those of the latter species were in the wall of the gall bladder and peritoneum. Spore development in plasmodia of these two species was synchronous. The spore body of H. ogawai sp. n. was 11.0 (8.9–12.2) μm in length, 6.9 (6.3–7.5) μm in width, 5.9 (5.2–6.6) μm in thickness, with a bifurcated caudal process of equal length, 10.0 (8.4–12.7) μm long; total spore length, 21.1 (19.2–23.4) μm. It contained two polar capsule, 4.3 (3.8–5.2) × 1.9 (1.4–2.3) μm. The spore body of H. yokoyamai sp. n. was 11.0 (10.1–13.7) μm in length, 7.1 (6.6–7.5) μm in width, and 5.6 (4.5–6.4) μm in thickness, with a bifurcated caudal process of equal length, 14.1 (10.8–17.0) μm long; total spore length, 25.0 (21.9–29.2) μm. It contained two polar capsules, 3.7 (3.1–4.2) × 2.0 (1.8–2.4) μm. A novel Myxobolus sp., Myxobolus machidai sp. n., is described from a spotted knifejaw (Oplegnathus punctatus) fished in the Sea of Japan, off Shimonoseki, Yamaguchi Prefecture, Japan. Plasmodia were embedded in the esophageal wall. Its round spore was small in size, 9.0 (8.1–9.4) μm in length, 7.8 (7.5–8.3) μm in width, and 5.5 (5.1–6.0) μm in thickness. It contained two polar capsules, 3.5 (3.2–3.8) × 2.3 (2.2–2.5) μm. Spore development in a plasmodium was asynchronous. Nucleotide sequencing of the small subunit ribosomal RNA gene (SSU rDNA) of these two novel Henneguya spp. revealed a close phylogenetic relationship with the marine clade of Henneguya spp.; however, they were distinct in morphology and SSU rDNA sequence from any known species. M. machidai sp. n. was grouped with freshwater Henneguya spp. in a phylogenetic tree based on the SSU rDNA, distant from a known marine clade of Myxobolus spp. reported mainly from the Mediterranean Sea. This is the first record of Henneguya–Myxobolus spp. from natural marine water in Japan.
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References
Andree KB, Szekely C, Molnar K, Gresoviac SJ, Hedrick RP (1999) Relationships among members of the genus Myxobolus (Myxozoa: Bilvalvulidae) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74
Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552
Bahri S, Andree KB, Hedrick RP (2003) Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. J Eukaryot Microbiol 50:463–470
Bahri S, Marton S, Marques A, Eszterbauer E (2010) Henneguya tunisiensis n. sp. (Myxosporea: Bivalvulida), a new gill parasite of Symphodus tinca (L.) (Teleostei: Labridae) off Tunisia. Syst Parasitol 76:93–101
Barassa B, Adriano EA, Cordeiro NS, Arana S, Ceccarelli PS (2012) Morphology and host–parasite interaction of Henneguya azevedoi n. sp., parasite of gills of Leporinus obtusidens from Mogi-Guaçu River, Brazil. Parasitol Res 110:887–894
Bartosová P, Fiala I, Hypsa V (2009) Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetixs. Mol Phylogenet Evol 53:81–93
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
Dyková I, De Buron I, Roumillat A, Fiala I (2011) Henneguya cynoscioni sp. n. (Myxosporea: Bivalvulida), an agent of severe cardiac lesions in the spotted seatrout, Cynoscion nebulosus (Teleostei: Sciaenidae). Folia Parasitol 58:169–177
Eiras JC (2002) Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 52:43–54
Eiras JC, Molnár K, Lu YS (2005) Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 61:1–46
Eszterbauer E (2004) Genetic relaionship among gill-infecting Myxobolus species (Myxosporea) of cypinids: molecular evidence of importance of tissue specificity. Dis Aquat Org 58:35–40
Feijó MM, Arana S, Ceccarelli PS, Adriano EA (2008) Light and scanning electron microscopy of Henneguya arapaima n. sp. (Myxoaoa: Myxobolidae) and histology of infected sites in pirarucu (Arapaima gigas: Pisces: Arapaimidae) from the Araguaia river, Brazil. Vet Parasitol 157:59–64
Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534
Fomena A, Bouix G (1996) New species of Henneguya Thélohan, 1892 (Myxozoa: Myxosporea) parasites of freshwater fishes in Cameroon. J Afr Zool 110:413–423
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Holzer AS, Sommerville C, Wootten R (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their SSU rDNA sequences. Int J Parasitol 34:1099–1111
Kaur H, Singh R (2011) Two new species of Myxobolus (Myxozoa: Myxosporea: Bivalvulida) infecting Indian freshwater fishes in Punjab Wetlands (India). Parasitol Res 108:1075–1082
Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffman RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413
Kopečná J, Jirku M, Oborník M, Tokarev YS, Lukes J, Modrý D (2006) Phylogenetic analysis of coccidian parasites from invertebrates: search for missing links. Protist 157:173–183
Kpatcha TK, Faye N, Diebakate C, Fall M, Toguebaye BS (1997) Nouvelles espèces d’ Henneguya Thélohan, 1895 (Myxozoa, Myxosporea) parasites des poisons marins du Sénégal: étude en microscopie photonique et électronique. Ann Sci Nat Zool 18:81–91
Liu Y, Whipps CM, Gu ZM, Zeng LB (2010) Myxobolus turpisrotundus (Myxosporea: Bivalvulida) spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence. Parasitol Res 107:699–706
Lom J (1969) A new taxonomic character in Myxosporidia, as demonstrated in description of two new species of Myxobolus. Folia Parasitol 16:97–103
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 (1994) Studies on protozoan parasites of Australian fishes. 3. Species of the genus Myxobolus Bütschli, 1882. Eur J Protistol 30:431–439
Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36
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 Y (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
Picon-Camacho SM, Holzer AS, Freeman MA, Morris DJ, Shinn AP (2009) Myxobolus albi n. sp. (Myxozoa) from the gills of the common goby Pomatoschistus microps Krøyer (Teleostei: Gobiidae). J Eukaryot Microbiol 56:421–427
Reed CC, Basson L, Van As LL, Dyková I (2007) Four new myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along the south coast of Africa. Folia Parasitol 54:283–292
Smythe AB, Sanderson MJ, Nadler SA (2006) Nematode small subunit phylogeny correlates with alignment parameters. Syst Biol 55:972–992
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
U-taynapum K, Penprapai N, Bangrak P, Mekata T, Itami T, Tantikitti C (2011) Myxobolus supamattayai n. sp. (Myxosporea: Myxobolidae) from Thailand parasitizing the scale pellicle of wild mullet (Valamugil seheli). Parasitol Res 109:81–91
Work TM, Takata G, Whipps CM, Kent ML (2008) A new species of Henneguya (Myxozoa) in the big-eyed scad (Selar crumenophthalmus) from Hawai. J Parasitol 94:524–529
Yokoyama H, Kawakami H, Yasuda H, Tanaka S (2003) Henneguya lateolabracis sp. n. (Myxozoa: Myxosporea), the causative agent of cardiac henneguyosis in Chinese sea bass Lateolabrax sp. Fish Sci 69:1116–1120
Yokoyama H, Itoh N, Tanaka S (2005) Henneguya pagri n. sp. (Myxozoa: Myxosporea) causing cardiac henneguyosis in red sea bream, Pagrus major (Temminck & Schlegel). J Fish Dis 28:479–487
Acknowledgments
This study was supported in part by a Grant-in-Aid (H23-shokuhin-ippan-007) from the Ministry of Health, Labour and Welfare of Japan.
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Li, YC., Sato, H., Kamata, Y. et al. Three novel myxobolid species of genera Henneguya and Myxobolus (Myxosporea: Bivalvulida) from marine fish in Japan. Parasitol Res 111, 819–826 (2012). https://doi.org/10.1007/s00436-012-2904-z
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DOI: https://doi.org/10.1007/s00436-012-2904-z