Parasitology Research

, Volume 112, Issue 4, pp 1737–1747 | Cite as

Kudoa azevedoi n. sp. (Myxozoa, Multivalvulida) from the oocytes of the Atlantic horse mackerel Trachurus trachurus (Perciformes, Carangidae) in Tunisian coasts

  • Lamjed Mansour
  • Aouatef Thabet
  • Kalthoum Chourabi
  • Abdul Halim Harrath
  • Mahr Gtari
  • Suliman Y. Al Omar
  • Oum Kalthoum Ben Hassine
Original Paper

Abstract

A new species Kudoa azevedoi sp. n. (Myxozoa, Multivalvulida) is described in Trachurus trachurus Linnaeus, 1758 (Carangidae) from fishing harbors in Tunisian coasts using spore morphology and SSU rDNA sequence data. The parasite occurs only in ovaries within oocytes of mature and immature specimens. Spores are quadrate in shape in apical view with rounded edges, having four shell valves and four symmetrical polar capsules. They are of small sizes and measure 3.5 ± 0.41 (3–4.2) × 4.5 ± 0.44 (4–5.2) length by width. The polar capsules are pyriform in shape measuring 1.5 ± 0.22 (1.5–2) × 0.75 ± 0.14 (0.5–1) μm. Infected oocytes are hypertrophied, whitish colored, and filled with mature spores. Plasmodia are tubular and ramified from the inner membrane toward the center of the oocyte. Phylogenetic analysis based on small subunit ribosomal DNA sequences shows the highest similarity (96 %) with the ovary parasite Kudoa ovivora. Some morphological details and spore dimensions support the creation of a new species in the genus Kudoa. Mean prevalence among examined females is of about 55.5 %. It varies between localities and length of fish. The present myxosporea is the second Kudoa species reported in fish ovaries.

Notes

Acknowledgments

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding the work through the research group project NoRGP-VPP-164

Declaration

All the experiments comply with the current laws of the country in which they were performed.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Abaunza P et al (2003) Growth and reproduction of horse mackerel, Trachurus trachurus (Carangidae). Rev Fish Biol Fish 13:27–61CrossRefGoogle Scholar
  3. Abdel-Ghaffar F, Bashtar AR, Mehlhorn H, Al-Rasheid K, Al-Olayan E, Abdel-Baki AA, Morsy K (2009) Ultrastructure and host parasite relationships of Kudoa pagrusi (Myxozoa) infecting the heart muscles of sea bream Pagrus pagrus (L.) from the Red Sea. Parasitol Res 106:121–129PubMedCrossRefGoogle Scholar
  4. Abdel-Ghaffar F, Morsy K, Mehlhorn H, Bashtar AR, Shazly MA, Saad AH, Abdel-Gaber R (2012) First report of Kudoa species (Myxozoa: Kudoidae) infecting the spotted coral grouper Plectropomus maculates from the Red Sea. A light and ultrastructural study. Parasitol Res 111:1579–1585PubMedCrossRefGoogle Scholar
  5. Al-Quraishy S, Koura E, Abdel-Baki A, Bashtar AR, El-Deed N, Al-Rasheid K, Abdel-Ghaffar F (2007) Light and electron microscopic studies on Kudoa pagrusi sp. n. (Myxosporea: Multivalvulida) infecting the heart of sea bream Pagrus pagrus (L.) from the Red Sea. Parasitol Res 102:205–209PubMedCrossRefGoogle Scholar
  6. Abollo E, Calvo M, Pascual S (2001) Hepatic coccidiosis of the blue whiting, Micromesistius poutassou (Risso), and horse mackerel, Trachurus trachurus (L.), from Galician waters. J Fish Dis 24:335–343CrossRefGoogle Scholar
  7. Adlard RD, Bryant MS, Whipps CM, Kent ML (2005) Multivalvulid myxozoans from eastern Australia: three new species of Kudoa from scombrid and labrid fishes of the Great Barrier Reef, Queensland, Australia. J Parasitol 91:1138–1142PubMedCrossRefGoogle Scholar
  8. Alvarez-Pellitero P, Sitja-Bobadilla A (1993) Pathology of myxosporea in marine fish culture. Dis Aquat Org 17:229–238CrossRefGoogle Scholar
  9. Aseeva NL (2004) New species of Myxosporea from genus Kudoa (Myxosporea, Multivalvulida) found in muscles of some fishes of the Sea of Japan. Vestn Zoologii 38:75–77Google Scholar
  10. Azevedo C, Matos E (2003) Amazonspora hassar n. gen. and n. sp. (phylum Microsporidia, fam. Glugeidae), a parasite of the Amazonian teleost Hassar orestis (fam. Doradidae). J Parasitol 89:336–341PubMedCrossRefGoogle Scholar
  11. Bekhti M, Bouix G (1985) Evolution of xenomas and the double role of polynuclear neutrophils in the microsporodiosis of Glugea stephani (Hagenmuller, 1899) in the flounder Platichthys flesus (Linne, 1758). Ann Parasitol Hum Comp 60:509–522PubMedGoogle Scholar
  12. Ben Salem M (1988) Régime alimentaire de Trachurus trachurus (Linnaeus, 1758) et de T. mediterraneus (Steindachner, 1868), (Poissons, Téléostéens, carangidae) de la province Atlantico-Mediterranéenne. Cybium 12:247–253Google Scholar
  13. Berrebi P (1979) Etude ultrastructurale de Glugea atherinae n. sp., microsporidie parasite de l’athérine Atherina boyeri Risso 1810 (poisson téléostéen) dans les lagunes du Languedoc et de Provence. Z Parasitenkd (Parasitol Res) 60:105–122CrossRefGoogle Scholar
  14. Blaylock RB, Bullard SA, Whipps CM (2004) Kudoa hypoepicardialis n. sp. (Myxozoa: Kudoidae) and associated lesions from the heart of seven perciform fishes in the northern Gulf of Mexico. J Parasitol 90:584–593PubMedCrossRefGoogle Scholar
  15. Burger MA, Adlard RD (2010) Four new species of Kudoa Meglitsch, 1947 (Myxosporea: Multivalvulida) from Australia with recommendations for species descriptions in the Kudoidae. Parasitology 137(5):793–814PubMedCrossRefGoogle Scholar
  16. Burger MA, Adlard RD (2011) Low host specificity in the Kudoidae (Myxosporea: Multivalvulida) including seventeen new host records for Kudoa thalassomi. Folia Parasitol (Praha) 58:1–16Google Scholar
  17. Campbell N (2005) The myxosporean parasitofauna of the Atlantic horse mackerel, Trachurus trachurus (L.) in the North-East Atlantic Ocean and Mediterranean Sea. Acta Parasitol 50:97–101Google Scholar
  18. Canning EU, Lom J (1986) The Microsporidia of vertebrates. Academic, New YorkGoogle Scholar
  19. Chatton E (1920) Un complexe xéno-parasitaire morphologique et physiologique Neresheimeria paradoxa chez Fritillaria pellucida. C R Acad Sci Paris 171:55–57Google Scholar
  20. Cho JB, Kim KH (2003) Light and electron-microscope description of Kudoa paralichthys n. sp. (Myxozoa, Myxosporea) from the brain of cultured olive flounder Paralichthys olivaceus in Korea. Dis Aquat Organ 55:59–63PubMedCrossRefGoogle Scholar
  21. Dyková I, Lom J (1987) Host cell hypertrophy induced by contact with trophozoites of Thelohanellus pyriformis (Myxozoa: Myxosporea). Arch Protistenkd 133:285–293CrossRefGoogle Scholar
  22. Dyková I, Tyml T, Kostka M (2011) Xenoma-like formations induced by Soricimyxum fegati (Myxosporea) in three species of shrews (Soricomorpha: Soricidae), including records of new hosts. Folia Parasitol (Praha) 58:249–256Google Scholar
  23. 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)CrossRefGoogle Scholar
  24. Egusa S (1986) The order Multivalvulida Shulman, 1959 (Myxozoa; Myxosporea): a review. Fish Pathol 21:261–274, in JapaneseCrossRefGoogle Scholar
  25. Egusa SN, 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 46:1193–1198CrossRefGoogle Scholar
  26. Friedrich C et al (2000) A myxozoan-like parasite causing xenomas in the brain of the mole, Talpa europaea L., 1758 (Vertebrata, Mammalia). Parasitology 121:483–492PubMedCrossRefGoogle Scholar
  27. Gaevskaya AV, Kovaleva AA (1979a) Two new species of myxosporidia from horse mackerel in the south eastern Atlantic. Biol Morya 3:80–83Google Scholar
  28. Gaevskaya AV, Kovaleva AA (1979b) New and rarely occurring Myxosporidia from Celtic Sea fishes. Parazitologiya 13:159–165Google Scholar
  29. Gaevskaya AV, Kovaleva AA (1982) The trematode fauna of Atlantic horse-mackerels of the genus Trachurus and its characteristics. Hydrobiol J 18:50–55Google Scholar
  30. Gaevskaya AV, Kovaleva AA (1985) The parasite fauna of the “oceanic horse mackerel” Trachurus picturatus picturatus and eco-geographical characteristics of its formation. Ekologiya Morya 20:80–84Google Scholar
  31. Grossel G (2005) Kudoa neurophila in striped trumpeter: identification, diagnostic development and histopathology. PhD thesis, University of Tasmania, p 137Google Scholar
  32. Grossel GW, Dyková I, Handlinger J, Munday BL (2003) Pentacapsula neurophila sp.n. (Multivalvulida) from the central nervous system of striped trumpeter, Latris lineata (Forster). J Fish Dis 26:315–320PubMedCrossRefGoogle Scholar
  33. Harada T, Kawai T, Sato H, Yokoyama H, Kumeda Y (2012) Development of a quantitative polymerase chain reaction assay for detection of Kudoa septempunctata in olive flounder (Paralichthys olivaceus). Int J Food Microbiol 156:161–167PubMedCrossRefGoogle Scholar
  34. Holzer AS, Blasco-Costa I, Sarabeev VL, Ovcharenko MO, Balbuena JA (2006) Kudoa trifolia sp. n. molecular phylogeny suggests a new spore morphology and unusual tissue location for a well-known genus. J Fish Dis 29:743–755PubMedCrossRefGoogle Scholar
  35. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877PubMedCrossRefGoogle Scholar
  36. Iwanowicz LR, Iwanowicz DD, Pote LM, Blazer VS, Schill WB (2008) Morphology and 18S rDNA of Henneguya gurlei (Myxosporea) from Ameiurus nebulosus (Siluriformes) in North Carolina. J Parasitol 94:46–57PubMedCrossRefGoogle Scholar
  37. Jardas I, Šantić M, Pallaoro A (2004) Diet composition and feeding intensity of horse mackerel, Trachurus trachurus (Osteichthyes: Carangidae) in the eastern Adriatic. Mar Biol 144:1051–1056CrossRefGoogle Scholar
  38. 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 59:2085–2091CrossRefGoogle Scholar
  39. Kawai T et al (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 54:1046–1052PubMedCrossRefGoogle Scholar
  40. Kovaleva AA (1970) Helminth fauna of mackerel of the genus Trachurus (Carangidae, Perciformes) in the Atlantic basin. Biol Morya 20:37–66Google Scholar
  41. Kovaleva AA, Gaevskaya AV (1984) New species of the genera Kudoa and Pentacapsula Myxosporidia. Multivalvulea with unusual location. Zool Zh 63:1090–1092Google Scholar
  42. Langdon JS (1991) Myoliquefaction post-mortem (‘milky flesh’) due to Kudoa thyrsites (Gilchrist) (Myxosporea: Multivalvulida) in mahi mahi, Coryphaena hippurus L. J Fish Dis 14:45–54CrossRefGoogle Scholar
  43. Lom J, Dyková I (2005) Microsporidian xenomas in fish seen in wider perspective. Folia Parasitol 52:69–81PubMedGoogle Scholar
  44. Lom J, Dyková I, Feist S (1989) Myxosporea-induced xenoma formation in pike (Esox lucius L.) renal corpuscles associated with Myxidium lieberkuehni infection. Eur J Protistol 24:271–280PubMedCrossRefGoogle Scholar
  45. Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156CrossRefGoogle Scholar
  46. Lom J, Dyková I (1992) Protozoan parasites of fishes. Elsevier, Amsterdam, p 315Google Scholar
  47. MacKenzie K, Campbell N, Mattiucci S, Ramos P, Pereira A, Abaunza P (2004) A checklist of the protozoan and metazoan parasites reported from the Atlantic horse mackerel, Trachurus trachurus (L.). Bull Eur Assoc Fish Path 24:180–184Google Scholar
  48. MacKenzie K, Campbell N, Mattiucci S, Ramos P, Pinto AL, Abaunza P (2008) Parasites as biological tags for stock identification of Atlantic horse mackerel Trachurus trachurus L. Fish Res 89:136–145CrossRefGoogle Scholar
  49. Mansour L, Prensier G, Jemaa SB, Hassine OK, Méténier G, Vivarès CP, Cornillot E (2005) Description of a xenoma-inducing microsporidian, Microgemma tincae n. sp., parasite of the teleost fish Symphodus tinca from Tunisian coasts. Dis Aquat Organ 65:217–226PubMedCrossRefGoogle Scholar
  50. 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 107:865–872PubMedCrossRefGoogle Scholar
  51. 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 108:913–926PubMedCrossRefGoogle Scholar
  52. Patashnik M, Groninger HS, Barnett H, Kudo G, Koury B (1982) Pacific whiting, Merluccius productus: I. Abnormal muscle texture caused by myxosporidian-induced proteolysis. Mar Fish Rev 44:1–12Google Scholar
  53. Mazza J (1963) Quelques trématodes de poissons de l’étang de Berre. Rev Trav de l’Inst Pêches Maritimes (ISTPM) 27:441–448Google Scholar
  54. 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 61:333–342PubMedCrossRefGoogle Scholar
  55. Smith-Vaniz WF (1986) Carangidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean, vol II. UNESCO, Paris, pp 815–844Google Scholar
  56. Moran JD, Margolis L, Webster JM, Kent ML (1999a) Development of Kudoa thyrsites (Myxozoa: Myxosporea) in netpen-reared Atlantic salmon determined by light microscopy and a polymerase chain reaction test. Dis Aquat Organ 37:185–193PubMedCrossRefGoogle Scholar
  57. Moran JDW, Whitaker DJ, Kent ML (1999b) A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172:163–196CrossRefGoogle Scholar
  58. Nikolaeva VM, Kovaleva AA (1966) Parasite fauna of Trachurus from the Mediterranean Basin. In: Delyamure SL (ed) Helminth fauna of animals in Southern Seas. Naukova Dumka, Kiev, pp 67–79Google Scholar
  59. Sandeep BV, Kalavati C, Narasimhamurti CC (1986) Kudoa atropisp sp.n. Myxosporea: Multivalvulida a myxosporidian parasite from the gills of Atropus atropus. Vestn Cesk Spol. Zool 50:132–135Google Scholar
  60. Sarkar NK, Mazumder SK (1983) Studies on myxosporidian parasites Myxozoa: Myxosporea from marine fishes in West Bengal, India: I. Description of three new species from Tachysurus spp. Arch Protistenkd 127:59–63CrossRefGoogle Scholar
  61. Saulnier D, Bremont M, de Kinkelin P (1996) Cloning, sequencing and expression of a cDNA encoding an antigen from the Myxosporean parasite causing the proliferative kidney disease of salmonid fish. Mol Biochem Parasitol 83:153–161PubMedCrossRefGoogle Scholar
  62. Schärer L, Vizoso DB (2003) Earlier sex change in infected individuals of the protogynous reef fish Thalassoma bifasciatum. Beh Ecol Soc 55:137–143CrossRefGoogle Scholar
  63. Stehr C, Whitaker DJ (1986) Host–parasite interaction of the myxosporeans Kudoa paniformis Kabata & Whitaker, 1981 and Kudoa thyrsites (Gilchrist, 1924) in the muscle of Pacific whiting, Merluccius productus (Ayres): an ultrastructural study. J Fish Dis 9:505–517CrossRefGoogle Scholar
  64. Swearer SE, Robertson DR (1999) Life history, pathology, and description of Kudoa ovivora n. sp. (Myxozoa, Myxosporea): an ovarian parasite of Caribbean labroid fishes. J Parasitol 85:337–353PubMedCrossRefGoogle Scholar
  65. Takvorian PM, Cali A (1986) The ultrastructure of spores (Protozoa: Microsporida) from Lophius americanus, the angler fish. J Protozool 33:570–575PubMedGoogle Scholar
  66. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  67. 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 25:4876–4882PubMedCrossRefGoogle Scholar
  68. Tsuyuki H, Williscroft SN, Kabata Z, Whitaker DJ (1982) The relationship between acid and neutral protease activities and the incidence of soft cooked texture in the muscle tissue of Pacific hake (Merluccius productus) infected with Kudoa paniformis and/or K. thyrsitis, held for varying times under different pre-fresh chilled storage conditions. Canadian technical report of fisheries and aquatic sciences. Dept. of Fisheries and Oceans, Fisheries Research Branch, Pacific Biological Station, 1130, p 39Google Scholar
  69. Van De Peer Y, De Wachter R (1997) Construction of evolutionary distance trees with TREECON for Windows: accounting for variation in nucleotide substitution rate among sites. Comput Appl Biosci 13:227–230PubMedGoogle Scholar
  70. Wang PC et al (2005) Systemic infection of Kudoa lutjanus n. sp. (Myxozoa: Myxosporea) in red snapper Lutjanus erythropterus from Taiwan. Dis Aquat Organ 67:115–124PubMedCrossRefGoogle Scholar
  71. Weissenberg R (1922) Mikrosporidien, Myxosporidien und Chlamydozoen als Zellparasiten von Fischen. Verh Dtsch Zool Ges 27:41–43Google Scholar
  72. Weissenberg R (1949) Cell growth and cell transformation induced by intracellular parasites. Anat Rec 103:101–102Google Scholar
  73. Weissenberg R (1968) Intracellular development of the microsporidan Glugea anomala Moniez in hypertrophying migratory cells of the fish Gasterosteus aculeatus L., an example of the formation of ‘xenoma’ tumors. I J Protozool 15:44–57Google Scholar
  74. Whipps CM et al (2004) Phylogeny of the multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. J Parasitol 90:618–622PubMedCrossRefGoogle Scholar
  75. Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Euk Microbiol 53:364–373PubMedCrossRefGoogle Scholar
  76. Whitaker DJ, Kent ML (1991) Myxosporean Kudoa thyrsites: a cause of soft flesh in farm-reared Atlantic salmon. J Aquat Anim Health 3:291–294CrossRefGoogle Scholar
  77. Yokoyama H, Yanagida T, Shirakashi S (2012) Kudoa ogawai n. sp. (Myxozoa: Multivalvulida) from the trunk muscle of Pacific barrelfish Hyperoglyphe japonica (Teleostei: Centrolophidae) in Japan. Parasitol Res 110:2247–2254PubMedCrossRefGoogle Scholar
  78. Yurakhno VM, Ovcharenko MO, Holzer AS, Sarabeev VL, Balbuena JA (2007) Kudoa unicapsula n. sp. (Myxosporea: Kudoidae) a parasite of the Mediterranean mullets Liza ramada and L. aurata (Teleostei: Mugilidae). Parasitol Res 101:1671–1680PubMedCrossRefGoogle Scholar
  79. Yurakhno VM (1988) On new myxosporidia of Black Sea fishes. Parazitologiya 22:521–524Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Lamjed Mansour
    • 1
  • Aouatef Thabet
    • 2
  • Kalthoum Chourabi
    • 2
  • Abdul Halim Harrath
    • 1
  • Mahr Gtari
    • 3
  • Suliman Y. Al Omar
    • 1
  • Oum Kalthoum Ben Hassine
    • 2
  1. 1.Zoology Department, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  2. 2.Unité de Recherche de Biologie Ecologie et Parasitologie des Organismes aquatiques, Département de Biologie, Faculté des Sciences de TunisUniversité de Tunis El-Manar TunisTunisTunisia
  3. 3.Maher Gtari, Laboratoire Microorganismes & Biomolécules Actives Université Tunis Elmanar (FST) & Université de Carthage (ISSTE)TunisTunisia

Personalised recommendations