Minchinia mercenariae n. sp. (Haplosporidia) in the hard clam mercenaria mercenaria: Implications of a rare parasite in a commercially important host

Journal of Eukaryotic Microbiology

Volumn 56, Issue 6, 2009, Pages 542-551

  Ford, Susan E ^a   Stokes, Nancy A ^b   Burreson, Eugene M ^b   Scarpa, Emily ^a   Carnegie, Ryan B ^b   Kraeuter, John N ^a   Bushek, David ^a  

^a RUTGERS UNIVERSITY   (United States)

^b VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

Author keywords

Aquaculture; Detection; Histology; In situ hybridization; Polymerase chain reaction; Quahog; Risk analysis

Indexed keywords

PROTOZOAL DNA; RIBOSOME RNA; SEA WATER;

BIVALVE; GENETIC ANALYSIS; HISTOLOGY; HISTOPATHOLOGY; IN SITU TEST; MOLLUSC CULTURE; NEW SPECIES; PARASITE; POLYMERASE CHAIN REACTION; PREDATION RISK; PROTIST; RISK ASSESSMENT; SCANNING ELECTRON MICROSCOPY; SPORE;

ANIMAL; AQUACULTURE; ARTICLE; CLASSIFICATION; DNA SEQUENCE; GENETICS; HAPLOSPORIDIA; HOST PARASITE INTERACTION; IN SITU HYBRIDIZATION; MERCENARIA; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE; UNITED STATES;

ANIMALS; AQUACULTURE; DNA, PROTOZOAN; HAPLOSPORIDA; HOST-PARASITE INTERACTIONS; IN SITU HYBRIDIZATION; MERCENARIA; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL; SEAWATER; SEQUENCE ANALYSIS, DNA; UNITED STATES;

FLORIDA [UNITED STATES]; MASSACHUSETTS; NEW JERSEY; NORTH AMERICA; UNITED STATES; VIRGINIA;

BACTERIA (MICROORGANISMS); BIVALVIA; HAPLOSPORIDIA; MERCENARIA; MERCENARIA MERCENARIA; MINCHINIA;

EID: 70350508197     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2009.00432.x     Document Type: Article

References (48)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W. Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res., 25 : 3389 3402.
2. Azevedo, C. 2001. Ultrastructural description of the spore maturation stages of the clam parasite Minchinia tapetis (Vilela, 1951) (Haplosporida: Haplosporidiidae). Syst. Parasitol., 49 : 189 194.
3. Azevedo, C. Corral, L. 1989. Fine structural observations of the natural spore excystment of Minchinia sp. (Haplosporida). Eur. J. Protistol., 24 : 168 173.
4. Azevedo, C., Corral, L. Perkins, F. O. 1985. Ultrastructural observations of spore excystment, plasmodial development and sporoblast formation in Haplosporidium lusitanicum (Haplosporida, Haplosporidiidae). Zeit. Parasit., 71 : 715 726.
5. Azevedo, C., Balseiro, P., Casal, G., Gestal, C., Aranguren, R., Stokes, N. A., Carnegie, R. B., Novoa, B., Burreson, E. M. Figueras, A. 2006. Ultrastructural and molecular characterization of Haplosporidium montforti n. sp., parasite of the European abalone Haliotis tuberculata. J. Invertebr. Pathol., 92 : 23 32.
6. Ball, S. J. 1980. Fine structure of the spores of Minchinia chitonis (Lankester, 1885) Labbé 1896 (Sporozoa: Haplosporida), a parasite of the chiton, Lepidochitona cinereus. Parasitology, 81 : 169 176.
7. Balouet, G., Poder, M. Cahour, A. 1983. Haemocytic parasitosis: morphology and pathology of lesions in the French flat oyster, Ostrea edulis L. Aquaculture, 34 : 1 14.
8. Bearham, D., Spiers, Z., Raidal, S., Jones, J. B. Nicholls, P. K. 2007. Molecular characterisation of a haplosporidian parasite infecting rock oysters Saccostrea cuccullata in north Western Australia. J. Invertebr. Pathol., 95 : 33 40.
9. Bearham, D., Spiers, Z., Raidal, S. R., Jones, J. B. Nicholls, P. K. 2008a. Spore ornamentation of Minchinia occulata n. sp. (Haplosporidia) in rock oysters Saccostrea cuccullata (Borne, 1778). Parasitology, 135 : 1271 1280.
10. Bearham, D., Spiers, Z., Raidal, S., Jones, J. B. Nicholls, P. K. 2008b. Detection of Minchinia sp., in rock oysters Saccostrea cuccullata (Born, 1778) using DNA probes. J. Invertebr. Pathol., 97 : 50 60.
11. Beauchamp, K. A., Kelley, G. O., El-Matbouli, M., Kathman, R. D., Nehring, R. B. Hedrick, R. P. 2002. Prevalence and susceptibility of infection to Myxobolus cerebralis, and genetic differences among populations of Tubifex tubifex. Dis. Aquat. Org., 51 : 113 121.
12. Burreson, E. M. Ford, S. E. 2004. A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquat. Liv. Res., 17 : 499 517.
13. Burreson, E. M., Robinson, M. E. Villalba, A. 1988. A comparison of paraffin histology and hemolymph analysis for the diagnosis of Haplosporidium nelsoni (MSX) in Crassostrea virginica (Gmelin). J. Shellfish Res., 7 : 19 24.
14. Burreson, E. M., Stokes, N. A. Friedman, C. S. 2000. Increased virulence in an introduced pathogen: Haplosporidium nelsoni (MSX) in the eastern oyster Crassostrea virginica. J. Aquat. Anim. Health, 12 : 1 8.
15. Burreson, E. M., Stokes, N. A., Carnegie, R. B. Bishop, M. J. 2004. Bonamia sp. (Haplosporidia) found in non-native oysters Crassostrea ariakensis in Bogue Sound, North Carolina. J. Aquat. Anim. Health, 16 : 1 9.
16. Carnegie, R. B., Burreson, E. M., Hine, P. M., Stokes, N. A., Audemard, C., Bishop, M. J. Peterson, C. H. 2006. Bonamia perspora n. sp. (Haplosporidia), a parasite of the oyster Ostreola equestris, is the first Bonamia species known to produce spores. J. Eukaryot. Microbiol., 53 : 232 245.
17. Dove, A. D. M., Bowser, P. R. Cerrato, R. M. 2004. Histological analysis of an outbreak of QPX disease in wild hard clams Mercenaria mercenaria in New York. J. Aquat. Anim. Health, 16 : 246 250.
18. Dykova, I., Lom, J. Fajer, E. 1988. A new haplosporean infecting the hepatopancreas in the penaeid shrimp, Penaeus vannamei. J. Invertebr. Pathol., 11 : 15 22.
19. Eversole, A. G. Heffernan, P. B. 1995. Gonandal neoplasia in northern Mercenaria mercenaria (Linneaeus, 1758), southern Mercenaria campechiensis (Gmelin, 1791) and their hybrids cultured in South Carolina. J. Shellfish Res., 14 : 33 39.
20. Farley, C. A. 1967. A proposed life cycle of Minchinia nelsoni (Haplosporida, Haplosporidiidae) in the American oyster Crassostrea virginica. J. Protozool., 14 : 616 625.
21. Ford, S. E. 2001. Pests, parasites, diseases, and defense mechanisms. In : Kraeuter, J. N. Castagna, M. (ed.), The Biology of the Hard Clam, Mercenaria Mercenaria (Linné). Elsevier Scientific Publishers, Amsterdam. p. 591 628.
22. Ford, S. E. Tripp, M. R. 1996. Diseases and Defense Mechanisms. In : Newell, R. I. E., Kennedy, V. S. Eble, A. F. (ed.), The Eastern Oyster Crassostrea Virginica. Maryland Sea Grant College, College Park, MD. p. 383 450.
23. Ford, S. E., Kraeuter, J. N., Barber, R. D. Mathis, G. 2002. Aquaculture associated factors in QPX disease of hard clams: density and seed source. Aquaculture, 208 : 23 38.
24. Ford, S. E., Smolowitz, R., Ragone-Calvo, L., Barber, R. D. Kraeuter, J. N. 1997. Evidence that QPX (Quahog Parasite Unknown) is not present in hatchery-produced hard clam seed. J. Shellfish Res., 16 : 519 521.
25. Friedman, C. S. 1996. Haplosporidian infections of the Pacific oyster, Crassostrea gigas (Thunberg), in California and Japan. J. Shellfish Res., 15 : 597 600.
26. Friedman, C. S., Cloney, D. F., Manzer, D. Hedrick, R. P. 1991. Haplosporidiosis of the Pacific oyster, Crassostrea gigas. J. Invertebr. Pathol., 58 : 367 372.
27. Gagne, N., Cochennec, N., Stephenson, M., McGladdery, S., Meyer, G. R. Bower, S. M. 2008. First report of a Mikrocytos-like parasite in European oysters Ostrea edulis from Canada after transport and quarantine in France. Dis. Aquat. Org., 80 : 27 35.
28. Hesselman, D. M., Blake, N. J. Peters, E. C. 1988. Gonadal neoplasms in hard shell clams Mercenaria spp., from the Indian River, Florida: occurrence, prevalence, and histopathology. J. Invertebr. Pathol., 52 : 436 446.
29. Kang, P. A. 1980. On the Minchinia sp. infection in the oysters from Chungmu area. Bull. Fish. Res. Dev. Agency, 25 : 25 28.
30. Kern, F. G. 1976. Sporulation of Minchinia sp. (Haplosporida, Haplosporidiidae) in the Pacific oyster Crassostrea gigas (Thunberg) from the Republic of Korea. J. Protozool., 23 : 498 500.
31. MacCallum, G. S. McGladdery, S. E. 2000. Quahog Parasite Unknown (QPX) in the northern quahog Mercenaria mercenaria (Linnaeus, 1758) and M. mercenaria var. notata from Atlantic Canada, survey results from three maritime provinces. J. Shellfish Res., 19 : 43 50.
32. McGovern, E. R. Burreson, E. M. 1990. Ultrastructure of Minchinia sp. spores from shipworms (Teredo spp.) in the western North Atlantic, with a discussion of taxonomy of the Haplosporidiidae. J. Protozool., 37 : 212 218.
33. Medlin, L., Elwood, H. J., Stickel, S. Sogin, M. L. 1988. The characterization of enzymatically amplified eukaryotic 16s-like rRNA-coding regions. Gene, 71 : 491 499.
34. Newman, M. W., Johnson, C. A. I. Pauley, G. B. 1976. A Minchinia-like haplosporidan parasitizing blue crabs, Callinectes sapidus. J. Invertebr. Pathol., 27 : 311 315.
35. Pichot, Y., Comps, M. Deltreil, J.-P. 1979. Recherches sur Haplosporidium sp. (Haplosporidia - Haplosporidiidae) parasite de l'huître plate Ostrea edulis. Rev. Trav. Inst. Pêches maritimes, 43 : 405 408.
36. Ragone Calvo, L. M., Walker, J. G. Burreson, E. M. 1998. Prevalence and distribution of QPX, Quahog Parasite Unknown, in hard clams, Mercenaria mercenaria, in Virginia, USA. Dis. Aquat. Org., 33 : 209 219.
37. Ragone Calvo, L. M., Ford, S. E., Kraeuter, J. N., Leavitt, D. F., Smolowitz, R. Burreson, E. M. 2007. Influence of host genetic origin and geographic location on QPX disease in hard clams, Mercenaria mercenaria. J. Shellfish Res., 26 : 109 119.
38. Reece, K. S., Siddall, M. E., Stokes, N. A., Bower, S. M. Burreson, E. M. 2004. Molecular phylogeny of Haplosporidia and characterization of unknown parasites. Cladistics, 20 : 93 94.
39. Renault, T., Stokes, N. A., Chollet, B., Cochennec, N., Berthe, F., Gerard, A. Burreson, E. M. 2000. Haplosporidiosis in the pacific oyster Crassostrea gigas from the French Atlantic coast. Dis. Aquat. Org., 42 : 207 214.
40. Shaw, B. L. Battle, H. I. 1957. The gross and microscopic anatomy of the digestive tract of the oyster Crassostrea virginica (Gmelin). Can. J. Zool., 35 : 325 347.
41. Smolowitz, R., Leavitt, D. Perkins, F. 1998. Observations of a protistan disease similar to QPX in Mercenaria mercenaria (hard clams) from the coast of Massachusetts. J. Invertebr. Pathol., 71 : 9 25.
42. Sprague, V. 1963. Minchinia louisiana n. sp. (Haplosporidia, Haplosporidiidae), a parasite of Panopeus herbstii. J. Protozool., 10 : 267 274.
43. Stokes, N. A. Burreson, E. M. 1995. A sensitive and specific DNA probe for the oyster pathogen Haplosporidium nelsoni. J. Eukaryot. Microbiol., 42 : 350 357.
44. Stokes, N. A. Burreson, E. M. 2001. Differential diagnosis of mixed Haplosporidium costale and Haplosporidium nelsoni infections in the eastern oyster, Crassostrea virginica, using DNA probes. J. Shellfish Res., 20 : 207 213.
45. * and Other Methods), Version 10. Sinauer Associates, Sunderland, MD.
46. van Banning, P. 1979. Haplosporidian diseases of imported oysters, Ostrea edulis, in Dutch estuaries. Mar. Fish. Rev., 41 : 8 18.
47. White, D. M. 2008. A molecular phylogeny of the genus Bonamia based on sequence data of the ribosomal RNA (rRNA) gene complex. Thesis. College of William and Mary, Williamsburg, VA. 78 p.
48. Wolf, K., Markiw, M. E. Hiltunen, J. K. 1986. Salmonid Whirling Disease - Tubifex tubifex (Muller) identified as the essential oligochete in the protozoan life-cycle. J. Fish Dis., 9 : 83 85.