Detection of Marteilia refringens using nested PCR and in situ hybridisation in Chamelea gallina from the Balearic Islands (Spain)

Diseases of Aquatic Organisms

Volumn 82, Issue 1, 2008, Pages 79-87

  López Flores, Inmaculada ^a   Robles, Francisca ^b   Valencia, José M ^c   Grau, Amalia ^c   Villalba, Antonio ^d   De La Herrán, Roberto ^b   Garrido Ramos, Manuel A ^b   Ruiz Rejón, Carmelo ^b   Ruiz Rejón, Manuel ^b   Navas, José I ^a  

^a IFAPA CENTRO EL TORUÑO   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c Govern Balear   (Spain)

^d CENTRO DE INVESTIGACIÓNS MARIÑAS   (Spain)

Author keywords

Chamelea gallina; IGS; Intergenic spacer; Marteilia refringens; Molecular diagnosis; rDNA

Indexed keywords

PROTOZOAL DNA; SPACER DNA;

BIOASSAY; BIVALVE; DETECTION METHOD; HYBRIDIZATION; MORTALITY; POLYMERASE CHAIN REACTION; PROTOZOAN;

ANIMAL; ARTICLE; BIVALVE; GENETICS; IN SITU HYBRIDIZATION; ISOLATION AND PURIFICATION; METHODOLOGY; PARASITOLOGY; POLYMERASE CHAIN REACTION; PROTOZOON; SPAIN;

ANIMALS; BIVALVIA; DNA, INTERGENIC; DNA, PROTOZOAN; IN SITU HYBRIDIZATION; POLYMERASE CHAIN REACTION; PROTOZOA; SPAIN;

BALEARIC ISLANDS; EURASIA; EUROPE; MEDITERRANEAN SEA; SOUTHERN EUROPE; SPAIN;

BIVALVIA; CHAMELEA GALLINA; MARTEILIA; MARTEILIA REFRINGENS;

EID: 56649086436     PISSN: 01775103     EISSN: 16161580     Source Type: Journal    
DOI: 10.3354/dao01966     Document Type: Article

References (61)

1. Adlard RD, Ernst I (1995) Extended range of the oyster pathogen, Marteilia sydneyi. Bull Eur Assoc Fish Pathol 15:119-121
2. Alderman DJ (1979) Epizootiology of Marteilia refringens in Europe. Mar Fish Rev 41:67-69
3. Anderson TJ, Lester RJG (1992) Sporulation of Marteilioides branchialis n. sp. (Paramyxea) in the Sydney rock oyster, Saccostrea commercialis: an electron microscope study. J Protozool 39:502-508
4. Audemard C, Le Roux F, Barnaud A, Collins C and others (2002) Needle in a haystack: involvement of the copepod Paracartia grani in the life-cycle of the oyster pathogen Marteilia refringens. Parasitology 124:315-323
5. Auffret M, Poder M (1983) Recherches sur Marteilia maurini, parasite de Mytilus edulis sur les côtes de Bretagne nord. Rev Trav Inst Pêch Marit 47:105-109
6. Balseiro P, Montes A, Ceschia G, Gestal C, Novoa B, Figueras A (2007) Molecular epizootiology of the European Marteilia spp., infecting mussels (Mytilus galloprovincialis and M. edulis) and oysters (Ostrea edulis): an update. Bull Eur Assoc Fish Pathol 27:148-156
7. Berthe FCJ, Le Roux F, Peyretaillade E, Peyret P, Rodriguez D, Gouy M, Vivares P (2000) Phylogenetic analysis of the small subunit ribosomal RNA of Marteilia refringens validates the existence of phylum Paramyxea (Desportes and Perkins, 1990). J Eukaryot Microbiol 47:288-293
8. Berthe FCJ, Le Roux F, Adlard RD, Figueras A (2004) Marteiliosis in molluscs: a review. Aquat Living Resour 17:433-448
9. Bigas M, Sagristà E, Bozzo G, Durfort M, Poquet M (2000) Ocurrence of heavy metals and protozoan parasites in the mussel, Mytilus galloprovincialis, collected in the western Mediterranean. Ecotoxicol Environ Saf 3:16-21
10. Bougrier S, Tigé G, Bachere E, Grizel H (1986) Ostrea angasi acclimatization to French coasts. Aquaculture 58:151-154
11. Butt D, Raftos DA (2007) Immunosuppression in Sydney rock oysters (Saccostrea glomerata) and QX disease in the Hawkesbury River, Sydney. J Mar Freshw Res 58:213-221
12. Cahour A (1979) Marteilia refringens and Crassostrea gigas. Mar Fish Rev 41:19-20
13. Carrasco N, López-Flores I, Alcaraz M, Furones MD, Berthe FCJ, Arzul I (2007a) First record of a Marteilia parasite (Paramyxea) in zooplankton populations from a natural estuarine environment. Aquaculture 269:63-70
14. Carrasco N, López-Flores I, Alcaraz M, Furones MD, Berthe FCJ, Arzul I (2007b) Dynamics of the parasite Marteilia refringens (Paramyxea) in Mytilus galloprovincialis and zooplankton populations in Alfacs Bay (Catalonia, Spain). Parasitology 134:1541-1550
15. Carrasco N, Arzul I, Chollet B, Robert M, Joly JP, Furones MD, Berthe FCJ (2008) Comparative experimental infection of the copepod Paracartia grani with Marteilia refringens and Marteilia maurini. J Fish Dis 31:497-504
16. Ceschia G, Zanchetta S, Sello M, Montes F, Figueras A (2001) Presenza di parassiti in cannolicchi (Ensis minor e Ensis siligua) pescati nell'area costiera del Mar Tirreno medidionale e del Mar Adriatico. Bol Soc Ital Pathol Ittica 13:20-27
17. Chatton E (1911) Sur une Cnidosporidie sans cnidoblaste (Paramyxa paradoxa, n. g., n. sp.). CR Acad Sci Paris 152:631-633
18. Comps M (1976) Marteilia lengehin. sp., parasite de l'huître Crassostrea cucullata Born. Rev Trav Inst Pêch Marit 40:347-349
19. Comps M (1983) Étude morphologique de Marteilia christenseni sp. n. parasite dulavignon Scrobicularia piperata P. (mollusque pélécypode). Rev Trav Inst Pêch Marit 47:99-104
20. Comps M, Joly JP (1980) Contamination expérimentale de Mytilus galloprovincialis Lmk par Marteilia refringens. Sci Pêche 301:19-21
21. Comps M, Grizel H, Tigé G, Duthoit JL (1975) Parasites nouveaux de la glande digestive des mollusques marins Mytilus edulis L. et Cardium edule. CR Acad Sci Paris Sér D 281:179-181
22. Comps M, Park MS, Desportes I (1986) Étude ultraestructurale de Marteilioides chungmuensis n. g., n. sp. parasite des ovocytes de l'huître Crassostrea gigas. Protistologica 22:279-285
23. Desportes I, Perkins FO (1990) Phylum Paramyxea. In: Margulis L, Corliss JO, Melkonian M, Chapman DJ (eds) Handbook of Protoctista. Jones and Barlett Publishing, Boston, MA, p 30-35
24. Durfort M (1994) Revisión de las parasitosis más frecuentes de los moluscos bivalvos de interés comercial del mar catalán (Mediterráneo). In: Castelló F, Calderer (eds) Actas del V Congreso Nacional de Acuicultura, May 10-13, 1995, S. Carlos de la Rápita, Spain, Universidad de Barcelona, p 52-62
25. Figueras AJ, Montes J (1988) Aber disease of edible oysters caused by Marteilia refringens. Am Fish Soc Spec Publ 18:38-46
26. Figueras A, Robledo JAF, Novoa B (1996) Brown ring disease and parasites in clams (Ruditapes decussatus and R. philippinarum) from Spain and Portugal. J Shellfish Res 15:363-368
27. Fuentes J, López JL, Mosquera E, Vázquez J, Villalba A, Álvarez G (2002) Growth, mortality, pathological conditions and protein expression of Mytilus edulis and M. galloprovincialis crosses cultured in the Ria de Arousa (NW of Spain). Aquaculture 213:233-251
28. Ginsburger-Vogel T (1991) Intersexuality in Orchestia mediterranea Costa, 1853, and Orchestia aestuarensis Wildish, 1987 (Amphipoda): a consequence of hybridisation or parasitic infestation? J Crustac Biol 11:530-539
29. Ginsburger-Vogel T, Desportes I, Zerbib C (1976) Présence chez l'amphipode Orchestia gammarellus (Pallas) d'un protiste parasite, ses affinités avec Marteilia refringens agent de l'épizootie de l'huître plate. CR Acad Sci Paris 283:939-942
30. Greer CE, Peterson SL, Kiviat NB, Manos MM (1991) PCR amplification from paraffin-embedded tissues - effects of fixative and fixation time. Am J Clin Pathol 95:117-124
31. Grizel H, Cops M, Bonami JR, Cousserans F, Duthoit JL, Le Pennec MA (1974) Recherche sur l'agent de la maladie de la glande digestive de Ostrea edulis Linné. Bull Inst Pêches Marit 240:7-30
32. Grizel H, Comps M, Raguenes D, Leborgne Y, Tigé G, Martin AG (1983) Bilan des essais d'acclimatation d'Ostrea chilensis sur les côtes de Bretagne. Rev Trav Inst Pêches Marit 46:209-225
33. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411-453
34. Itoh N, Momoyama K, Ogawa K (2005) First report of three protozoan parasites (a haplosporidian, Marteilia sp. and Marteilioides sp.) from the Manila clam, Venerupis (=Ruditapes) philippinarum in Japan. J Invertebr Pathol 88:201-206
35. Karagiannis D, Angelidis P (2007) Infection of cultured mussels Mytilus galloprovincialis by the protozoan Marteilia sp. in the Thermaikos Gulf (N Greece). Bull Eur Assoc Fish Pathol 27:131-141
36. Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111-120
37. Kleeman SN, Le Roux F, Berthe F, Adlard RD (2002) Specificity of PCR and in situ hybridisation assays designed for detection of Marteilia sydneyi and M. refringens. Parasitology 125:131-141
38. Kumar S, Tamura K, Jakobsen IB, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetic analysis and sequence alignment. Brief Bioinform 5:150-163
39. Larsson JIR, Køie M (2005) Ultrastructural study and description of Paramyxoides nephtys gen. n. sp. n. a parasite of Nephtys caeca (Fabricius, 1780) (Polychaeta: Nephtyidae). Acta Protozool 44:175-187
40. Le Roux F, Audemard C, Barnaud A, Berthe F (1999) DNA probes as potential tools for the detection of Marteilia refringens. Mar Biotechnol 1:588-597
41. Le Roux F, Lorenzo G, Peyret P, Audemard C and others (2001) Molecular evidence for the existence of two species of Marteilia in Europe. J Eukaryot Microbiol 48:449-454
42. Lee MK, Cho BY, Lee SY, Kang JY, Joeng HD, Huh SH, Huh MD (2001) Histopathological lesions of Manila clam, Tapes philippinarum, from Hadong and Namhae coastal areas of Korea. Aquaculture 201:199-209
43. López-Flores I, de la Herran R, Garrido-Ramos MA, Navas JI, Ruiz-Rejón C, Ruiz-Rejón M (2004) The molecular diagnosis of Marteilia refringens and differentiation between Marteilia strains infecting oysters and mussels based on the rDNA IGS sequence. Parasitology 129:411-419
44. López-Flores I, Garrido-Ramos MA, de la Herran R, Ruiz-Rejón C, Ruiz-Rejón M, Navas JI (2008) Identification of Marteilia refringens infecting the razor clam Solen marginatus by PCR and in situ hybridization. Mol Cell Probes 22:151-155
45. Moyer MA, Blake NJ, Arnold WS (1993) An ascetosoporan disease causing mass mortality in the Atlantic calico scallop, Argopecten gibbus (Linnaeus, 1758). J Shellfish Res 12:305-310
46. Ngo TTT, Berthe FCJ, Choi KS (2003) Prevalence and infection intensity of the ovarian parasite Marteilioides chungmuensis during an annual reproductive cycle of the oyster Crassostrea gigas. Dis Aquat Org 56:259-267
47. Norton JH, Perkins FP, Ledua E (1993) Marteilia-like infection in a giant clam Tridacna maxima in Fiji. J Invertebr Pathol 61:328-330
48. Novoa B, Posada D, Figueras A (2005) Polymorphisms in the sequences of Marteilia internal transcribed spacer region of the ribosomal RNA genes (ITS-1) in Spain: genetic types are not related with bivalve hosts. J Fish Dis 28:331-338
49. Pascual M, Martin AG, Zampatti E, Coatanea D, Defossez J, Robert R (1991) Testing of the Argentina oyster, Ostrea puelchana, in several French oyster farming sites. ICES CM/K:30. ICES, Copenhagen
50. Perkins F, Wolf P (1976) Fine structure of Marteilia sydneyi sp. n. Haplosporidian pathogen of Australian oysters. J Parasitol 62:528-538
51. Poder M, Auffret M, Balouet G (1983) Études pathologiques et épidémiologiques des lésions parasitaires chez Ostrea edulis L. Premiers résultants d'une recherche prospective comparative chez les principales espèces de mollusques des zones ostréicoles de Bretagne nord. In: Colloques sur les bases biologiques de l'aquaculture, Dec 12-16. CNRS-CNEXO, Montpellier, p 125-138
52. Renault T, Cochennec N, Chollet B (1995) Marteiliosis in American oysters Crassostrea virginica reared in France. Dis Aquat Org 23:161-164
53. Robert R, Borel M, Pichot Y, Trut G (1991) Growth and mortality of the European oyster Ostrea edulis in the Bay of Arcachon (France). Aquat Living Resour 4:265-274
54. Taveekijakarn P, Nash G, Somsiri T, Putinaowarat S (2002) Marteilia-like species: first report in Thailand. AAHRI Newsl 11:1-2
55. Tige G, Rabouin MA (1976) Étude d'un lot de moules transférées dans un centre touché par l'épizootie affectant l'huître plate. ICES CM/K:21. ICES, Copenhagen
56. Tun KL, Itoh N, Komiyama H, Ueki N, Yoshinaga T, Ogawa K (2006) Comparison of Marteiloides chungmuensis infection in the Pacific oyster Crassostrea gigas cultured in different conditions. Aquaculture 253:91-97
57. Villalba A, Mourelle SG, Carballal MJ, Lopez MC (1993a) Effects of infection by the protistan parasite Marteilia refringens on the reproduction of cultured mussels Mytilus galloprovincialis in Galicia (NW Spain). Dis Aquat Org 17:205-213
58. Villalba A, Mourelle SG, Lopez MC, Carballal MJ, Azevedo C (1993b) Marteiliasis affecting cultured mussels Mytilus galloprovinciaäs of Galicia (NW Spain). I. Etiology, phases of the infection and temporal and spatial variability in prevalence. Dis Aquat Org 16:61-72
59. Villalba A, López MC, Carballal MJ (1993c) Parásitas y alteraciones patológicas de tres especies de almeja, Ruditapes decussatus, Venerupis pullastra y Venerupis rhomboides, en las rías gallegas. In: Cervino A, Landin A, de Coo A, Guerra A, Torres M (eds) Actas IV Congreso Nacional de Acuicultura. Centro de Investigacións Mariñas, Vilanova de Arousa, p 551-556
60. Wilson IG (1997) Inhibition and facilitation of nucleic acid amplification. Appl Environ Microbiol 63:3741-3751
61. Zrncic S, Le Roux F, Oraic D, Sostaric B, Berthe FCJ (2001) First record of Marteilia sp. in mussels Mytilus galloprovincialis in Croatia. Dis Aquat Org 44:143-148