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Myxobolus musseliusae (Myxozoa: Myxobolidae) from the gills of common carp Cyprinus carpio and revision of Myxobolus dispar recorded in China

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Abstract

During a survey of myxozoan parasites of common carp Cyprinus carpio in Honghu Lake, Hubei Province, China, a parasite was collected that was identified as Myxobolus dispar based on an earlier description from China. However, the small subunit ribosomal DNA of this species shared only 90 % similarity with M. dispar, instead matching M. musseliusae with 100 % identity. To resolve this apparent taxonomic conflict, the validity of M. dispar reported from China was investigated. The species encountered here and in the earlier report from China both bear spores that are notably smaller than those of M. dispar in Europe. In the present study, a mucous envelope was adhered to the posterior of many fresh spores and was observed to expand and surround the spore. This structure has never been reported from fresh spores of M. dispar. Histology showed extravascular plasmodia in the gill filaments in close contact with the cartilaginous ray of the filament, which contrasts with the plasmodia of M. dispar which develop in the arteries of the gill filaments. Phylogenetically, the current species is distinct from M. dispar, instead forming a sister group with M. musseliusae. The data presented here allow us to conclude that the species isolated is M. musseliusae and that prior reports of M. dispar in China are unsubstantiated.

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References

  • Adriano EA, Arana S, Alves AL, Silva MR, Ceccarelli PS, Henrique-Silva F, Maia AA (2009) Myxobolus cordeiroi n. sp., a parasite of Zungaro jahu (Siluriformes: Pimelodiade) from Brazilian Pantanal: morphology, phylogeny and histopathology. Vet Parasitol 162:221–229

    Article  PubMed  CAS  Google Scholar 

  • American Fisheries Society (2004) Guidelines for the use of fishes in research. Bethesda: American Fisheries Society. http://fisheries.org/docs/policy_useoffishes.pdf

  • Andree KB, Székely C, Molnár 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

    Article  PubMed  CAS  Google Scholar 

  • Chen QL, Ma CL (1998) Myxozoa: Myxosporea. Science, Beijing, In Chinese

    Google Scholar 

  • Dayoub A, Molnár K, Salmanl H, Al-Samman A, Székely C (2007) Myxobolus infections of common carp (Cyprinus carpio) in Syrian fish farms. Acta Vet Hung 55:501–509

    Article  PubMed  Google Scholar 

  • Dyková I, Lom J (2007) Histopathology of protistan and myxozoan infections in fishes. Academia, Prague, p 219

    Google Scholar 

  • Eszterbauer E, Székely C (2004) Molecular phylogeny of the kidney parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp. from goldfish (Carassius auratus auratus). Acta Vet Hung 52:469–478

    Article  PubMed  CAS  Google Scholar 

  • Eszterbauer E, Benkő M, Dán Á, Molnár K (2001) Identification of fish parasitic Myxobolus (Myxosporea) species using a combined PCR-RFLP method. Dis Aquat Org 44:35–39

    Article  PubMed  CAS  Google Scholar 

  • Ferguson JA, Atkinson SD, Whipps CM, Kent ML (2008) Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of Myxobolus fryeri n. sp. J Parasitol 94:1322–1334

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Ivasik VM, Gevkan II, Vorona NJ (1967) Gill myxosporeosis in carp. Zool Zh 46:941–943 (In Russian)

    Google Scholar 

  • Liu Y, Gu ZM, Luo YL (2010a) Some additional data to the occurrence, morphology and validity of Myxobolus turpisrotundus Zhang, 2009 (Myxozoa: Myxosporea). Parasitol Res 107:67–73

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Whipps CM, Gu ZM, Zeng LB (2010b) 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

    Article  PubMed  Google Scholar 

  • Liu Y, Gu ZM, Zhang YC, Zeng LB (2011a) Redescription and molecular analysis of Myxobolus shantungensis Hu, 1965 (Myxozoa: Myxosporea) infecting common carp Cyprinus carpio haematopterus. Parasitol Res 109:1619–1623

    Article  PubMed  Google Scholar 

  • Liu Y, Whipps CM, Gu ZM, Zeng C, Huang MJ (2011b) Myxobolus honghuensis n. sp. (Myxosporea: Bivalvulida) parasitizing the pharynx of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) from Honghu Lake, China. Parasitol Res. doi:10.1007/s00436-011-2629-4

  • Lom J, Arthur JR (1989) A guideline for preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156

    Article  Google Scholar 

  • Lom J, Dyková I (1992) Protozoan parasites of fishes. Developments in aquaculture and fisheries science, vol 26. Elsevier, Amsterdam, 315 pp

    Google Scholar 

  • Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36

    PubMed  Google Scholar 

  • Molnár K (1994) Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitol Hung 27:5–20

    Google Scholar 

  • Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Org 48:197–207

    Article  PubMed  Google Scholar 

  • Molnár K (2011) Remarks to the validity of Genbank sequences of Myxobolus spp. (Myxozoa, Myxosporidae) infecting Eurasian fishes. Acta Parasitol 56:263–269

    Article  Google Scholar 

  • Molnár K, Szakolczai J (1980) Halbetegségek. Mezőgazdasági Kiadó, Budapest, p 254 (in Hungarian)

  • Molnár K, Eszterbauer E, Székely C, Dan A, Harrach B (2002) Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. J Fish Dis 25:643–652

    Article  Google Scholar 

  • Molnár K, Székely C, Hallett SL, Atkinson SD (2009) Some remarks on the occurrence, host-specificity and validity of Myxobolus rotundus Nemeczek, 1911 (Myxozoa: Myxosporea). Syst Parasitol 72:71–79

    Article  PubMed  Google Scholar 

  • Molnár K, Marton S, Székely C, Eszterbauer E (2010) Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitol Res 107:1137–1150

    Article  PubMed  Google Scholar 

  • Molnár 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. Parasitol Res 79:109–121

    Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Parker JD, Warner MC (1970) Effects of fixation, dehydration and staining on dimensions of myxosporidian and microsporidian spores. J Wildl Dis 6:448–459

    PubMed  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Salim KY, Desser SS (2000) Descriptions and phylogenetic systematics of Myxobolus spp. from cyprinids in Algonquin Park, Ontario. J Eukaryot Microbiol 47:309–318

    Article  PubMed  CAS  Google Scholar 

  • Székely C, Shaharom-Harrison F, Cech G, Ostoros G, Molnár K (2009) Myxozoan infections in fishes of the Tasik Kenyir Water Reservoir, Terengganu, Malaysia. Dis Aquat Org 83:37–48

    Article  PubMed  Google Scholar 

  • Thélohan P (1895) Recherches sur les Myxosporidies. Bull Sci Fr Belg 26:100–394

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Whipps CM, El-Matbouli M, Hedrick RP, Blazer V, Kent ML (2004) Myxobolus cerebralis internal transcribed spacer 1 (ITS-1) sequences support recent spread of the parasite to North America and within Europe. Dis Aquat Org 60:105–108

    Article  PubMed  CAS  Google Scholar 

  • Yakovchuk TA (1979) A new species of the genus Myxobolus (Myxosporidia, Myxobolidae) from the gill filaments of the carp. Parazitologiya 13:635–636

    Google Scholar 

  • Zhang JY, Yokoyama H, Wang JG, Li AH, Gong XN, Ryu-Hasegawa A, Iwashita M, Ogawa K (2010) Utilization of tissue habitats by Myxobolus wulii Landsberg & Lom, 1991 in different carp hosts and disease resistance in allogynogenetic gibel carp: redescription of M. wulii from China and Japan. J Fish Dis 33:57–68

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y, Sun C, Kent ML, Deng J, Whipps CM (2008) Description of a new species of Myxobolus (Myxozoa: Myxobolidae) based on morphological and molecular data. J Parasitol 94:737–742

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Gao Yu (College of Fisheries, Huazhong Agricultural University) for his help with the drawing of spores and Xiao Peng (Institute of Hydrobiology, Chinese Academy of Sciences) for providing the applied microscope. The authors are also thankful to Edit Eszterbauer (Veterinary Medical Research Institute, Hungarian Academy of Sciences) for providing helpful suggestions on this article. This study was supported by the Nature Science Foundation of China (project numbers 31172052 and 30800096), the Science Fund for Distinguished Young Scholars of Hubei Province (project number 2011CDA091), the New Teacher Foundation of Chinese Education Department (project number 200805041025), the Huazhong Agricultural University Scientific & Technological Self-innovation Foundation (project number 2009SC017), the Fundamental research funds for the central universities (project numbers 2011PY011 and 2012PY004), and the Technology Project for strengthening innovation of Yunnan Province (project number 2009AD009). The Hungarian partner was financed by the grant OTKA, project no. K71837.

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Correspondence to Z. M. Gu.

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Liu, Y., Whipps, C.M., Gu, Z.M. et al. Myxobolus musseliusae (Myxozoa: Myxobolidae) from the gills of common carp Cyprinus carpio and revision of Myxobolus dispar recorded in China. Parasitol Res 112, 289–296 (2013). https://doi.org/10.1007/s00436-012-3136-y

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