1887

Abstract

Gregarines are thought to be deep-branching apicomplexans. Accordingly, a robust inference of gregarine phylogeny is crucial to any interpretation of apicomplexan evolution, but molecular sequences from gregarines are restricted to a small number of small-subunit (SSU) rDNA sequences from derived taxa. This work examines the usefulness of SSU rDNA and β-tubulin sequences for inferring gregarine phylogeny. SSU rRNA genes from (Mingazzini) sp., Stein, Clopton and Dufour, as well as the β-tubulin gene from , were sequenced. The results of phylogenetic analyses of alveolate taxa using both genes were consistent with an early origin of gregarines and the putative ‘sister’ relationship between gregarines and , but neither phylogeny was strongly supported. In addition, two SSU rDNA sequences from unidentified marine eukaryotes were found to branch among the gregarines: one was a sequence derived from the haemolymph parasite of the giant clam, , and the other was a sequence misattributed to the foraminiferan . In all of our analyses, the SSU rDNA sequence from sp. clustered weakly with the apicomplexans, which is consistent with ultrastructural data. Altogether, the exact position of gregarines with respect to and other apicomplexans remains to be confirmed, but the congruence of SSU rDNA and β-tubulin trees with one another and with morphological data does suggest that further sampling of molecular data will eventually put gregarine diversity into a phylogenetic context.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.02284-0
2003-01-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/53/1/ijs530345.html?itemId=/content/journal/ijsem/10.1099/ijs.0.02284-0&mimeType=html&fmt=ahah

References

  1. Barta, J. R. ( 1989; ). Phylogenetic analysis of the class Sporozoea (phylum Apicomplexa Levine, 1970) : evidence for the independent evolution of heteroxenous life cycles. J Parasitol 75, 195–206.[CrossRef]
    [Google Scholar]
  2. Barta, J. R., Jenkins, M. C. & Danforth, H. D. ( 1991; ). Evolutionary relationships of avian Eimeria species among other Apicomplexan protozoa: monophyly of the apicomplexa is supported. Mol Biol Evol 8, 345–355.
    [Google Scholar]
  3. Belton, P. & Grundfest, H. ( 1962; ). Potassium activation and K+ spikes in muscle fibers of mealworm larva (Tenebrio molitor). Am J Physiol 203, 588–594.
    [Google Scholar]
  4. Black, M. W. & Boothroyd, J. C. ( 2000; ). Lytic cycle of Toxoplasma gondii. Microbiol Mol Biol Rev 64, 607–623.[CrossRef]
    [Google Scholar]
  5. Brugerolle, G. & Mignot, J. P. ( 1979; ). Observations sur le cycle l'ultrastructure et la position systematique de Spiromonas perforans (Bodo perforans Hoolande 1938), flagelle parasite de Chilomonas paramecium: ses relations avec les dinoflagelles et sporozoaires. Protistologica 15, 183–196.
    [Google Scholar]
  6. 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.[CrossRef]
    [Google Scholar]
  7. 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.[CrossRef]
    [Google Scholar]
  8. Cavalier-Smith, T. ( 1993; ). Kingdom Protozoa and its 18 phyla. Microbiol Rev 57, 953–994.
    [Google Scholar]
  9. Clopton, R. E. ( 1995; ). Leidyana migrator n. sp. (Apicomplexa, Eugregarinida, Leidyanidae) from the Madagascar hissing cockroach, Gromphadorhina portentosa (Insecta, Blattodea). Invertebr Biol 114, 271–278.[CrossRef]
    [Google Scholar]
  10. Clopton, R. E. & Janovy, J. ( 1993; ). Developmental niche structure in the gregarine assemblage parasitizing Tenebrio molitor. J Parasitol 79, 701–709.[CrossRef]
    [Google Scholar]
  11. Clopton, R. E., Percival, T. J. & Janovy, J. ( 1991; ). Gregarine niphandrodes, n. sp. (Apicomplexa: Eugregarinorida) from adult Tenebrio molitor (L.) with oocyst descriptions of other gregarine parasites of the yellow mealworm. J Protozool 38, 472–479.[CrossRef]
    [Google Scholar]
  12. Clopton, R. E., Janovy, J., Jr & Percival, T. J. ( 1992; ). Host stadium specificity in the gregarine assemblage parasitizing Tenebrio molitor. J Parasitol 78, 334–337.[CrossRef]
    [Google Scholar]
  13. Cox, F. E. G. ( 1994; ). The evolutionary expansion of the Sporozoa. Int J Parasitol 24, 1301–1316.[CrossRef]
    [Google Scholar]
  14. Díez, B., Pedrós-Alió, C. & Massana, R. ( 2001; ). Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67, 2932–2941.[CrossRef]
    [Google Scholar]
  15. Dodge, J. D. & Crawford, R. M. ( 1971; ). Fine structure of the dinoflagellate Oxyrrhis marina. I. The general structure of the cell. Protistologica 7, 339–409.
    [Google Scholar]
  16. Ellis, J. & Morrison, D. ( 1995; ). Effects of sequence alignment on the phylogeny of Sarcocystis deduced from 18S rDNA sequences. Parasitol Res 81, 696–699.[CrossRef]
    [Google Scholar]
  17. Ellis, J., Hefford, C., Baverstock, P. R., Dalrymple, B. P. & Johnson, A. M. ( 1992; ). Ribosomal DNA sequence comparison of Babesia and Theileria. Mol Biochem Parasitol 54, 87–95.[CrossRef]
    [Google Scholar]
  18. Ellis, T. J., Luton, K., Baverstock, P. R., Whitworth, G., Tenter, A. M. & Johnson, A. M. ( 1995; ). Phylogenetic relationships between Toxoplasma and Sarcocystis deduced from a comparison of 18S rDNA sequences. Parasitology 110, 521–528.[CrossRef]
    [Google Scholar]
  19. Ellis, J. T., Morrison, D. A. & Jeffries, A. C. ( 1998; ). The phylum Apicomplexa: an update on the molecular phylogeny. In Evolutionary Relationships Among Protozoa, pp. 255–274. Edited by G. H. Coombs, K. Vickerman, M. A. Sleigh & A. Warren. Boston: Kluwer.
  20. Escalante, A. A. & Ayala, F. J. ( 1994; ). Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci U S A 91, 11373–11377.[CrossRef]
    [Google Scholar]
  21. 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.[CrossRef]
    [Google Scholar]
  22. 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.[CrossRef]
    [Google Scholar]
  23. Felsenstein, J. ( 1993; ). phylip (Phylogeny Inference Package). Distributed by the author. Department of Genetics, University of Washington, Seattle, USA.
  24. Fernández, I., Pardos, F., Benito, J. & Arroyo, N. L. ( 1999; ). Acrocoelus glossobalani gen. nov. et sp. nov., a protistan flagellate from the gut of the enteropneust Glossabalanus minutus. Eur J Protistol 35, 55–65.[CrossRef]
    [Google Scholar]
  25. Foissner, W. & Foissner, I. ( 1984; ). First record of an ectoparasitic flagellate of ciliates: an ultrastructural investigation of the morphology and the mode of attachment of Spiromonas gonderi nov. spec. (Zoomastigophora, Spiromonadidae) invading the pellicle of ciliates of the genus Colpoda (Ciliophora, Colpodidae). Protistologica 20, 635–648.
    [Google Scholar]
  26. Gajadhar, A. A., Marquardt, W. C., Hall, R., Gunderson, J., Ariztia-Carmona, E. V. & Sogin, M. L. ( 1991; ). Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. Mol Biochem Parasitol 45, 147–154.[CrossRef]
    [Google Scholar]
  27. Goggin, C. L. & Barker, S. C. ( 1993; ). Phylogenetic position of the genus Perkinsus (Protista, Apicomplexa) based on small subunit ribosomal RNA. Mol Biochem Parasitol 60, 65–70.[CrossRef]
    [Google Scholar]
  28. Hnida, J. A. & Duszynski, D. W. ( 1999; ). Taxonomy and systematics of some Eimeria species of murid rodents as determined by the ITS1 egion of the ribosomal gene complex. Parasitology 119, 349–357.[CrossRef]
    [Google Scholar]
  29. Hoffman, E. G. & Yancey, R. M. ( 1966; ). Ellobiopsidae of Alaskan coastal waters. Pacific Sci 20, 70–78.
    [Google Scholar]
  30. Holmdahl, O. J., Morrison, D. A., Ellis, J. T. & Huong, L. T. ( 1999; ). Evolution of ruminant Sarcocystis (Sporozoa) parasites based on small subunit rDNA sequences. Mol Phylogenet Evol 11, 27–37.[CrossRef]
    [Google Scholar]
  31. Johnson, A. M., Fielke, R., Lumb, R. & Baverstock, P. R. ( 1990; ). Phylogenetic relationships of Cryptosporidium determined by ribosomal RNA sequence comparison. Int J Parasitol 20, 141–147.[CrossRef]
    [Google Scholar]
  32. Keeling, P. J., Luker, M. A. & Palmer, J. D. ( 2000; ). Evidence from beta-tubulin phylogenies that microsporidia evolved from within the fungi. Mol Biol Evol 17, 23–31.[CrossRef]
    [Google Scholar]
  33. Kozloff, E. N. ( 1983; ). Seashore Life of the Northern Pacific Coast, 2nd edn. Seattle: University of Washington Press.
  34. Levine, N. D. ( 1970; ). Taxonomy of the Sporozoa. J Parasitol 56, 208–209.
    [Google Scholar]
  35. Levine, N. D. ( 1971; ). Taxonomy of the Archigregarinorida and Selenidiidae (Protozoa, Apicomplexa). J Protozool 18, 704–717.[CrossRef]
    [Google Scholar]
  36. Levine, N. D. ( 1976; ). Revision and checklist of the species of the aseptate gregarine genus Lecudina. Trans Am Microsc Soc 95, 695–702.[CrossRef]
    [Google Scholar]
  37. Levine, N. D. ( 1985; ). Phylum Apicomplexa Levine 1970 . In An Illustrated Guide to the Protozoa, pp. 322–374. Edited by J. J. Lee, S. H. Hutner & E. C. Bovee. Lawrence, KS: Society of Protozoologists.
  38. Levine, N. D. ( 1988; ). The Protozoan Phylum Apicomplexa. Boca Raton, FL: CRC Press.
  39. López-García, P., Rodriguez-Valera, F., Pedrós-Alió, C. & Moreira, D. ( 2001; ). Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409, 603–607.[CrossRef]
    [Google Scholar]
  40. Maddison, D. R. & Maddison, W. P. ( 2000; ). MacClade. Sunderland, MA: Sinauer.
  41. McLaughlin, R. E. & Myers, J. ( 1970; ). Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of the monarch butterfly D. gilippus berenice Cramer. J Protozool 17, 300–305.[CrossRef]
    [Google Scholar]
  42. Meier, M. ( 1956; ). Die Monocystideenfauna der Oligochaten von Erlangen und Umgebung. Arch Protistenkd 101, 335–400.
    [Google Scholar]
  43. Mignot, J. P. & Brugerolle, G. ( 1975; ). Etude ultrastructurale de flagelle phagotrophe Colponema loxodes Stein. Protistologica 11, 429–444.
    [Google Scholar]
  44. Moon-van der Staay, S. Y., De Wachter, R. & Vaulot, D. ( 2001; ). Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409, 607–610.[CrossRef]
    [Google Scholar]
  45. Morgan, U. M., Monis, P. T., Fayer, R., Deplazes, P. & Thompson, R. C. ( 1999; ). Phylogenetic relationships among isolates of Cryptosporidium: evidence for several new species. J Parasitol 85, 1126–1133.[CrossRef]
    [Google Scholar]
  46. 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.[CrossRef]
    [Google Scholar]
  47. Norén, F., Moestrup, Ø. & Rehnstam-Holm, A.-S. ( 1999; ). Parvilucifera infectans Norén et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Eur J Protistol 35, 233–254.[CrossRef]
    [Google Scholar]
  48. Patterson, D. ( 1999; ). The diversity of eukaryotes. Am Nat 154, 96–124.[CrossRef]
    [Google Scholar]
  49. Pawlowski, J., Bolivar, I., Fahrni, J. F., Cavalier-Smith, T. & Gouy, M. ( 1996; ). Early origin of Foraminifera suggested by SSU rRNA gene sequences. Mol Biol Evol 13, 445–450.[CrossRef]
    [Google Scholar]
  50. Perkins, F. O. ( 1976; ). Zoospores of the oyster pathogen, Dermocystidium marinum. I. Fine structure of the conoid and other sporozoan-like organelles. J Parasitol 62, 959–974.[CrossRef]
    [Google Scholar]
  51. Perkins, F. O. ( 1996; ). The structure of Perkinsus marinus (Mackin, Owen and Collier, 1950) Levine, 1978 with comments on the taxonomy and phylogeny of Perkinsus spp. J Shellfish Res 15, 67–87.
    [Google Scholar]
  52. Reece, K. S., Siddall, M. E., Burreson, E. M. & Graves, J. E. ( 1997; ). Phylogenetic analysis of Perkinsus based on actin gene sequences. J Parasitol 83, 417–423.[CrossRef]
    [Google Scholar]
  53. Siddall, M. E. ( 1995; ). Phylogeny of adeleid blood parasites with a partial systematic revision of the haemogregarine complex. J Eukaryot Microbiol 42, 116–125.[CrossRef]
    [Google Scholar]
  54. Siddall, M. E. & Barta, J. R. ( 1992; ). Phylogeny of Plasmodium species: estimation and inference. J Parasitol 78, 567–568.[CrossRef]
    [Google Scholar]
  55. Siddall, M. E., Reece, K. S., Graves, J. E. & Burreson, E. M. ( 1997; ). ‘Total evidence’ refutes the inclusion of Perkinsus species in the phylum Apicomplexa. Parasitology 115, 165–176.[CrossRef]
    [Google Scholar]
  56. Siddall, M. E., Reece, K. S., Nerad, T. A. & Burreson, E. M. ( 2001; ). Molecular determination of the phylogenetic position of a species in the genus Colpodella (Alveolata). Am Mus Novit 3314, 1–10.[CrossRef]
    [Google Scholar]
  57. Simpson, A. G. B. & Patterson, D. J. ( 1996; ). Ultrastructure and identification of the predatory flagellate Colpodella pugnax Cienkowski (Apicomplexa) with a description of Colpodella turpis n. sp. and a review of the genus. Syst Parasitol 33, 187–198.[CrossRef]
    [Google Scholar]
  58. Strimmer, K. & Von Haeseler, A. ( 1996; ). Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13, 964–969.[CrossRef]
    [Google Scholar]
  59. Swofford, D. L. ( 1999; ). paup* 4.0. Phylogenetic analysis using parsimony (and other methods). Sunderland, MA: Sinauer.
  60. Théodoridés, J. ( 1984; ). The phylogeny of the Gregarinia. Orig Life 13, 339–342.[CrossRef]
    [Google Scholar]
  61. Van de Peer, Y., Caers, A., De Rijk, P. & De Wachter, R. ( 1998; ). Database on the structure of small ribosomal subunit RNA. Nucleic Acids Res 26, 179–182.[CrossRef]
    [Google Scholar]
  62. Vivier, E. & Desportes, I. ( 1990; ). Phylum Apicomplexa. In The Handbook of Protoctista, pp. 549–573. Edited by L. Margulis, J. O. Corliss, M. Melkonian & D. J. Chapman. Boston: Jones and Bartlett.
  63. Whisler, H. C. ( 1990; ). Incertae Sedis: Ellobiopsida. In The Handbook of Protoctista, pp. 715–716. Edited by L. Margulis, J. O. Corliss, M. Melkonian & D. J. Chapman. Boston: Jones and Bartlett.
  64. Wolters, J. ( 1991; ). The troublesome parasites – molecular and morphological evidence that Apicomplexa belong to the dinoflagellate–ciliate clade. Biosystems 25, 75–83.[CrossRef]
    [Google Scholar]
  65. Wray, C. G., Langer, M. R., DeSalle, R., Lee, J. J. & Lipps, J. H. ( 1995; ). Origin of the foraminifera. Proc Natl Acad Sci U S A 92, 141–145.[CrossRef]
    [Google Scholar]
  66. Zhu, G., Keithly, J. S. & Philippe, H. ( 2000; ). What is the phylogenetic position of Cryptosporidium? Int J Syst Evol Microbiol 50, 1673–1681.[CrossRef]
    [Google Scholar]
  67. Zolan, M. E. & Pukkila, P. J. ( 1986; ). Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6, 195–200.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.02284-0
Loading
/content/journal/ijsem/10.1099/ijs.0.02284-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error