1887

Abstract

The eugregarines are a group of apicomplexan parasites that mostly infect the intestines of invertebrates. The high level of morphological variation found within and among species of eugregarines makes it difficult to find consistent and reliable traits that unite even closely related lineages. Based mostly on traits observed with light microscopy, the majority of described eugregarines from marine invertebrates has been classified into a single group, the Lecudinidae. Our understanding of the overall diversity and phylogenetic relationships of lecudinids is very poor, mainly because only a modest amount of exploratory research has been done on the group and very few species of lecudinids have been characterized at the molecular phylogenetic level. In an attempt to understand the diversity of marine gregarines better, we surveyed lecudinids that infect the intestines of Pacific ascidians (i.e. sea squirts) using ultrastructural and molecular phylogenetic approaches; currently, these species fall within one genus, . We collected lecudinid gregarines from six ascidian host species, and our data demonstrated that each host was infected by a different species of : (i) sp. nov., isolated from , (ii) sp. nov., isolated from , (iii) sp. nov., isolated from , (iv) sp. nov., isolated from , (v) cf. , isolated from , and (vi) sp. nov., isolated from . Visualization of the trophozoites with scanning electron microscopy showed that four of these species were covered with epicytic folds, whereas two of the species were covered with a dense pattern of epicytic knobs. The molecular phylogenetic data suggested that species of with surface knobs form a clade that is nested within a paraphyletic assemblage species of with epicytic folds.

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2015-08-01
2024-04-23
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References

  1. Cavalier-Smith T. ( 2014;). Gregarine site-heterogeneous 18S rDNA trees, revision of gregarine higher classification, and the evolutionary diversification of Sporozoa. Eur J Protistol 50 472495 [View Article] [PubMed].
    [Google Scholar]
  2. Ciancio A., Scippa S., Cammarano M. ( 2001;). Ultrastructure of trophozoites of the gregarine Lankesteria ascidiae (Apicomplexa: Eugregarinida) parasitic in the ascidian Ciona intestinalis (Protochordata). Eur J Protistol 37 327336 [View Article].
    [Google Scholar]
  3. Desportes I., Schrével J. ( 2013). Treatise on Zoology – Anatomy, Taxonomy, Biology. The Gregarines: The Early Branching Apicomplexa Leiden: Brill;. [CrossRef]
    [Google Scholar]
  4. Dyakin A.Y., Simdyanov T.G. ( 2005;). The cortical zone of skittle-like cells of Urospora chiridotae, a gregarine from an apode holothuria Chiridota laevis . Protistology 4 97105.
    [Google Scholar]
  5. Edgar R.C. ( 2004;). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 17921797 [View Article] [PubMed].
    [Google Scholar]
  6. Grassé P.-P. ( 1953;). Classe des grégarinomorphes (Gregarinomorpha, n. nov., Gregarinae Haeckel, 1866; Gregarinidea Lankester, 1885; grégarines des auteurs). . In Traité de Zoologie, pp. 590690. Edited by Grassé P.-P. Paris: Masson; (in French) .
    [Google Scholar]
  7. Huelsenbeck J.P., Ronquist F. ( 2001;). mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17 754755 [View Article] [PubMed].
    [Google Scholar]
  8. Kimura M. ( 1980;). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16 111120 [View Article] [PubMed].
    [Google Scholar]
  9. Landers S.C., Leander B.S. ( 2005;). Comparative surface morphology of marine coelomic gregarines (Apicomplexa, Urosporidae): Pterospora floridiensis Pterospora schizosoma . J Eukaryot Microbiol 52 2330 [View Article] [PubMed].
    [Google Scholar]
  10. Leander B.S. ( 2008;). Marine gregarines: evolutionary prelude to the apicomplexan radiation?. Trends Parasitol 24 6067 [View Article] [PubMed].
    [Google Scholar]
  11. Leander B.S., Clopton R.E., Keeling P.J. ( 2003;). Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and β-tubulin. Int J Syst Evol Microbiol 53 345354 [View Article] [PubMed].
    [Google Scholar]
  12. Leander B.S., Lloyd S.A.J., Marshall W., Landers S.C. ( 2006;). Phylogeny of marine Gregarines (Apicomplexa) – Pterospora Lithocystis Lankesteria – and the origin(s) of coelomic parasitism. Protist 157 4560 [View Article] [PubMed].
    [Google Scholar]
  13. Levine N.D. ( 1976;). Revision and checklist of the species of the aseptate gregarine genus Lecudina . Trans Am Microsc Soc 95 695702 [View Article] [PubMed].
    [Google Scholar]
  14. Levine N.D. ( 1977;). Revision and checklist of the species (other than Lecudina) of the aseptate gregarine family Lecudinidae. J Protozool 24 4152 [View Article] [PubMed].
    [Google Scholar]
  15. Levine N.D. ( 1979;). New genera and higher taxa of septate gregarines (Protozoa, Apicomplexa). J Protozool 26 532536 [View Article].
    [Google Scholar]
  16. Levine N.D. ( 1981;). New species of Lankesteria (Apicomplexa, Eugregarinida) from ascidians on the central California coast. J Protozool 28 363370 [View Article].
    [Google Scholar]
  17. Levine N.D. ( 1988;). Progress in taxonomy of the apicomplexan protozoa. J Protozool 35 518520 [View Article] [PubMed].
    [Google Scholar]
  18. Maddison D.R., Maddison W.P. ( 2005). MacClade 4.08 Sunderland, MA: Sinauer Associates;.
    [Google Scholar]
  19. Mingazzini P. ( 1891;). Le gregarine monocistidee dei tunicati e della capitella. Atti R Accad Lincei 7 407414 (in Italian) .
    [Google Scholar]
  20. Mita K., Kawai N., Rueckert S., Sasakura Y. ( 2012;). Large-scale infection of the ascidian Ciona intestinalis by the gregarine Lankesteria ascidiae in an inland culture system. Dis Aquat Organ 101 185195 [View Article] [PubMed].
    [Google Scholar]
  21. Ormières R. ( 1965;). Recherches sur les sporozoaires parasites de tuniciers. Vie Milieu 15 823946 (in French) .
    [Google Scholar]
  22. Ormières R. ( 1972;). Études ultrastructurale des Lankesteria, eugrégarines parasites de tunicieres. Comparison avec les ‘Lankesteria’ parasites des diptères. C R Hebd Seances Acad Sci 274 32543257 (in French) .
    [Google Scholar]
  23. Perkins F.O., Barta J.R., Clopton R.E., Pierce M.A., Upton S.J. ( 2000;). Phylum Apicomplexa. . In The Illustrated Guide to the Protozoa, pp. 190304. Edited by Lee J. J., Leedale G. F., Bradbury P. Lawrence, KS: Allen Press;.
    [Google Scholar]
  24. Posada D., Crandall K.A. ( 1998;). modeltest: testing the model of DNA substitution. Bioinformatics 14 817818 [View Article] [PubMed].
    [Google Scholar]
  25. Reichenow E. ( 1953). Doflein's Lehrbuch der Protozoenkunde Jena: Gustav Fischer; (in German) .
    [Google Scholar]
  26. Rueckert S., Leander B.S. ( 2008;). Morphology and phylogenetic position of two novel marine gregarines (Apicomplexa, Eugregarinorida) from the intestines of North-eastern Pacific ascidians. Zool Scr 37 637645 [View Article].
    [Google Scholar]
  27. Rueckert S., Chantangsi C., Leander B.S. ( 2010;). Molecular systematics of marine gregarines (Apicomplexa) from North-eastern Pacific polychaetes and nemerteans, with descriptions of three novel species: Lecudina phyllochaetopteri sp. nov., Difficilina tubulani sp. nov. and Difficilina paranemertis sp. nov.. Int J Syst Evol Microbiol 60 26812690 [View Article] [PubMed].
    [Google Scholar]
  28. Rueckert S., Villette P.M.A.H., Leander B.S. ( 2011a;). Species boundaries in gregarine apicomplexan parasites: a case study-comparison of morphometric and molecular variability in Lecudina cf. tuzetae (Eugregarinorida, Lecudinidae). J Eukaryot Microbiol 58 275283 [View Article] [PubMed].
    [Google Scholar]
  29. Rueckert S., Simdyanov T.G., Aleoshin V.V., Leander B.S. ( 2011b;). Identification of a divergent environmental DNA sequence clade using the phylogeny of gregarine parasites (Apicomplexa) from crustacean hosts. PLoS One 6 e18163 [View Article] [PubMed].
    [Google Scholar]
  30. Simdyanov T.G. ( 1995;). [The ultrastructure of two species of gregarines of the genus Lankesteria (Eugregarinida: Lecudinidae)]. Parazitologiia 29 424432 (in Russian) .
    [Google Scholar]
  31. 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 27312739 [View Article] [PubMed].
    [Google Scholar]
  32. Théodoridès J. ( 1967;). Sur la position systématique du genre Lankesteria Mingazzini, 1891 (Eugregarina). C R Acad Sci Hebd Seances Acad Sci D 265 19951996 (in French) .
    [Google Scholar]
  33. Valigurová A., Vaškovicová N., Musilová N., Schrével J. ( 2013;). The enigma of eugregarine epicytic folds: where gliding motility originates?. Front Zool 10 57 [View Article] [PubMed].
    [Google Scholar]
  34. Vávra J. ( 1969;). Lankesteria barretti n. sp. (Eugregarinida, Diplocystidae), a parasite of the mosquito Aedes triseriatus (Say) and a review of the genus Lankesteria Mingazzini. J Protozool 16 546570 [View Article] [PubMed].
    [Google Scholar]
  35. Votýpka J., Lantová L., Ghosh K., Braig H., Volf P. ( 2009;). Molecular characterization of gregarines from sand flies (Diptera: Psychodidae) and description of Psychodiella n.g. (Apicomplexa: Gregarinida). J Eukaryot Microbiol 56 583588 [View Article] [PubMed].
    [Google Scholar]
  36. Wakeman K., Leander B.S. ( 2013;). Identity of environmental DNA sequences using descriptions of four novel marine gregarine parasites, Polyplicarium n. gen. (Apicomplexa), from capitellid polychaetes. Mar Biodiv 43 133147 [View Article].
    [Google Scholar]
  37. Ward R.N., Levine N.D., Craig J.G.B. ( 1953;). Ascogregarina nom. nov. for Ascocystis Grassé. Journal of Parasitology 68 331. [CrossRef]
    [Google Scholar]
  38. Zwickl D. ( 2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion PhD thesis, University of Texas at Austin, Austin, TX, USA .
    [Google Scholar]
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