Cellular identity of a novel small subunit rDNA sequence clade of Apicomplexans: Description of the marine parasite Rhytidocystis polygordiae n. sp. (Host: Polygordius sp., Polychaeta)

Journal of Eukaryotic Microbiology

Volumn 53, Issue 4, 2006, Pages 280-291

  Leander, Brian S ^a   Ramey, Patricia A ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Agamococcidia; Apicomplexa; Apicoplast; Archiannelids; Coccidia Cryptosporidium; Gregarines; Molecular phylogeny; Rhytidocystis; Ultrastructure

Indexed keywords

PROTOZOAL DNA; RIBOSOME DNA; RIBOSOME RNA; SEA WATER;

DNA; ELECTRON MICROSCOPY; NEW GENUS; NEW SPECIES; PARASITE; PHYLOGENETICS;

ANIMAL; APICOMPLEXA; ARTICLE; CLASSIFICATION; CYTOLOGY; GENETICS; INTESTINE; PARASITOLOGY; PHYLOGENY; POLYCHAETA; RNA GENE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; APICOMPLEXA; DNA, PROTOZOAN; DNA, RIBOSOMAL; GENES, RRNA; INTESTINES; MICROSCOPY, ELECTRON, TRANSMISSION; PHYLOGENY; POLYCHAETA; RNA, RIBOSOMAL; SEAWATER;

ATLANTIC OCEAN; NORTH AMERICA;

APICOMPLEXA; BIVALVIA; CONOIDEA; MONOCYSTIDAE; POLYCHAETA; POLYGORDIUS; TRIDACNA CROCEA; TUBULOCRISTATA;

EID: 33745619229     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2006.00109.x     Document Type: Article

References (56)

1. Beyer, T. V., Svezhova, N. V., Radchenko, A. I. & Sidorenko, N. V. 2002. Parasitophorous vacuole: morphofunctional diversity in different coccidian genera (a short insight into the problem). Cell Biol. Int., 26:861-871.
2. Bruno, W. J., Socci, N. D. & Halpern, A. L. 2000. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol., 17:189-197.
3. Carreno, R. A., Martin, D. S. & Barta, J. R. 1999. Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitol. Res., 85:899-904.
4. Cavalier-Smith, T. & Chao, E. E. 2004. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur. J. Protistol., 40:185-212.
5. Chen, X.-M., Keithly, J. S., Paya, C. V. & LaRusso, N. F. 2002. Cryptosporidiosis. N. Engl. J. Med., 346:1723-1731.
6. Cox, F. E. G. 1994. The evolutionary expansion of the sporozoa. Int. J. Parasitol., 24:1301-1316.
7. de Beauchamp, P. 1913. Recherches sur les Rhytidocystis parasities des Ophélies. Arch. Protistenkd., 31:138-168.
8. Desportes, I. 1969. Ultrastructure et developement des gregarines du genre Stylocephalus. Ann. Sci. Nat. Zool., 11:31-96.
9. Elliot, D. A. & Clark, D. P. 2000. Cryptosporidium parvum induces host-cell actin accumulation at the host-parasite interface. Infect. Immun., 68:2315-2322.
10. Fast, N. M., Kissinger, J. C., Roos, D. S. & Keeling, P. J. 2001. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol., 18:418-426.
11. Fast, N. M., Xue, L., Bingham, S. & Keeling, P. J. 2002. Re-examining alveolate evolution using multiple protein molecular phylogenies. J. Eukaryot. Microbiol., 49:30-37.
12. Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package). University of Washington, Seattle.
13. Giard, A. 1880. On the affinities of the genus Polygordius with the annelids of the family Opheliidae. Ann. Mag. Nat. Hist., 6:324-326.
14. Grassé, P.-P. 1953. Classe des grégarinomorphes (Gregarinomorpha n. nov.; Gregarinae Haeckel, 1866; gregarinidea Lankester, 1885; grégarines des auteurs). In: Grassé, P.-P. (ed.), Traité de Zoologie. Masson, Paris. p. 590-690.
15. Harper, J. T., Waanders, E. & Keeling, P. J. 2005. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int. J. Syst. Evol. Microbiol., 55:487-496.
16. Hennig, W. 1966. Phylogenetic Systematics. University of Illinois Press, London.
17. Huelsenbeck, J. P. & Ronquist, F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17:754-755.
18. Kuvardina, O. N., Leander, B. S., Aleshin, V. V., Myl'nikov, A. P., Keeling, P. J. & Simdyanov, T. G. 2002. The phylogeny of colpodellids (Eukaryota, Alveolata) using small subunit rRNA genes suggests they are the free-living ancestors of apicomplexans. J. Eukaryot. Microbiol., 49:498-504.
19. Landers, S. C. 2002. The fine structure of the gamont of Pterospora floidiensis (Apicomplexa: Eugregarinida). J. Eukaryot. Microbiol., 49:220-226.
20. Lang-Unnasch, N., Reith, M. E., Munholland, J. & Barta, J. R. 1998. Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int. J. Parasitol., 28:1743-1754.
21. Leander, B. S. & Keeling, P. J. 2003. Morphostasis in alveolate evolution. Trends Ecol. Evol., 18:395-402.
22. Leander, B. S., Clopton, R. E. & Keeling, P. F. 2003a. Phylogeny of gregarines (Apicomplexa) as inferred from SSU rDNA and beta-tubulin. Int. J. Syst. Evol. Microbiol., 53:345-354.
23. Leander, R. S., Harper, J. T. & Keeling, P. J. 2003b. Molecular phylogeny and surface morphology of marine aseptate gregarines (Apicomplexa): Selenidium spp. and Lecudina spp. J. Parasitol., 89:1191-1205.
24. Leander, B. S., Kuvardina, O. N., Aleshin, V. V., Mylnikov, A. P. & Keeling, P. J. 2003c. Molecular phylogeny and surface morphology of Colpodella edax (Alveolata): insights into the phagotrophic ancestry of apicomplexans. J. Eukaryot. Microbiol., 50:334-340.
25. Leander, B. S. & Keeling, P. J. 2004. Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from hsp90 and actin phylogenies. J. Phycol., 40:341-350.
26. Leander, B. S., Lloyd, S. A. J., Marshall, W. & Landers, S. C. 2006. Phylogeny of marine gregarines (Apicomplexa) - Pterospora, Lithocystis and Lankesteria - and the origin(s) of coelomic parasitism. Protist, 157:45-60.
27. Levine, N. D. 1979. Agamococcidiorida ord. n. and Rhytidocystidae fam. n. for the coccidian genus Rhytidocystis Henneguy, 1907. J. Protozool., 26:167-168.
28. Levine, N. D. 1988. The Protozoan Phylum Apicomplexa. CRC Press Inc., Boca Raton, FL.
29. Maddison, D. R. & Maddison, W. P. 2000. MacClade. Sinauer Associates Inc., Sunderland, MA.
30. McFadden, G. I. 2003. Plastids, mitochondria and hydrogenosomes. In: Marr, J. J., Nielsen, T. W. & Komuniecki, R. (ed.), Molecular Medical Parasitology. Academic Press, Boston. p. 277-294.
31. McFadden, G. I., Waller, R. F., Reith, M. E. & Lang-Unnasch, N. 1997. Plastids in apicomplexan parasites. In: Bhattacharya, D. (ed.), Plant Systematics and Evolution. Springer Verlag, Berlin. p. 261-287.
32. McIntosh, W. C. 1875. On a new example of the Opheliidae Linotrypane apogon from Shetland. Proc. Royal Soc. Edinburgh, 8:386-390.
33. Morrissette, N. S. & Sibley, L. D. 2002. Cytoskeleton of apicomplexan parasites. Microbiol. Mol. Biol. Rev., 66:21-38.
34. Nakayama, K., Nishijima, M. & Maruyama, T. 1998. Parasitism by a protozoan in the hemolymph of the giant clam, Tridacna crocea. J. Invertebr. Pathol., 71:193-198.
35. Oborník, M., Jirku, M., Slapeta, J. R., Modry, D., Koudela, B. & Lukeš, J. 2002. Notes on coccidian phylogeny, based on the apicoplast small subunit ribosomal DNA. Parasitol. Res., 88:360-363.
36. Petry, F. 2004. Structural analysis of Cryptosporidium parvum. Microsc. Microanal., 10:586-601.
37. Porchet-Hennere, E. 1972. Observations en microscopie photonique et electronique sur la sporogenese de Dehornia (1) sthenelais (n. gen., sp. n.), sporozoaire parasite de l'annedlide polychaete Sthenelais boa (Aphroditides). Protistologica, 8:245-255.
38. Posada, D. & Crandall, K. A. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics, 14:817-818.
39. Ramey, P. A., Fiege, D. & Leander, B. S. 2006. A new species of Polygordius (Polychaeta: Polygordiidae): a dominant member of infaunal communities on the inner continental shelf and in bays and harbors of the northeastern United States. J. Mar. Biol. Assoc. UK, (in press)
40. Rouse, G. W. & Pleijel, F. 2001. Polychaetes. Oxford University Press, London.
41. Schrével, J. 1968. L'ultrastructure de la région antérieure de la grégarine Selenidium et son intérêt pour l'étude de la nutrition chez les sporozoaires. J. Microsc., 7:391-410.
42. Schrével, J. 1971a. Observations biologiques et ultrastructurales sur les Selenidiidae et leurs conséquences sur la systématique des grégarinomorphes. J. Protozool., 18:448-470.
43. Schrével, J. 1971b. Contribution a l'étude des Selenidiidae parasites d'annélides polychètes. II Ultrastructure de quelques trophozoïtes. Protistologica, 7:101-130.
44. Sheffield, H. G., Garnham, P. C. C. & Shiroishi, T. 1971. The fine structure of the sporozoite of Lankesteria culcis. J. Protozool., 18:98-105.
45. Strimmer, K. & Von Haeseler, A. 1996. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol., 13:964-969.
46. Swofford, D. L. 1999. Phylogenetic Analysis Using Parsimony (and Other Methods) PAUP* 4.0. Sinauer Associates Inc., Sunderland, MA.
47. Upton, S. J. & Peters, E. C. 1986. A new and unusual species of coccidium (Apicomplexa: Agamococcidiorida) from Jamaican scleractinian corals. J. Invertebr. Pathol., 47:184-193.
48. Vivier, E. 1968. L'organization ultrastructurale corticale de la gregarine Lecudina pellucida: ses repports avec l'alimentation et la locomotion. J. Protozool., 15:230-246.
49. Vivier, E. & Desportes, I. 1990. Phylum Apicomplexa. In: Margulis, L., Corliss, J. O., Melkonian, M. & Chapman, D. J. (ed.), The Handbook of Protoctista. Jones & Bartlett Publishers, Boston. p. 549-573.
50. Vivier, E. & Hennere, E. 1965. Ultrastructure des stades végétatifs de la coccidie Coelotropha durchoni. Protistologica, 1:89-104.
51. Vivier, E. & Schrével, J. 1966. Les ultrastructures cytoplasmiques de Selenidium hollandei, n. sp. grégarine parasite de Sabellaria alveolata L. J. Microsc., 5:213-228.
52. Von Alt, C. J. & Grassle, J. F. 1992. LEO-15, an unmanned long-term environmental observatory. Proc. Oceans '92, 2:849-854.
53. Waller, R. F. & McFadden, G. I. 2005. The apicoplast: a review of the derived plastid of apicomplexan parasites. Curr. Issues Mol. Biol., 7:57-80.
54. Warner, F. D. 1968. The fine structure of Rhynchocystis pilosa (Sporozoa, Eugregarinida). J. Protozool., 15:59-73.
55. Wray, C. G., Langer, M. R., DeSalle, R., Lee, J. J. & Lipps, J. H. 1995. Origin of the foraminifera. Proc. Natl. Acad. Sci. USA, 92:141-145.
56. Zhu, G., Marchewka, M. J. & Keithly, J. S. 2000. Cryptosporidium parvum appears to lack a plastid genome. Microbiology, 146:315-321.