Parasitology Research

, Volume 111, Issue 3, pp 1331–1342 | Cite as

Phylogeny of fish-infecting Calyptospora species (Apicomplexa: Eimeriorina)

  • Christopher M. Whipps
  • John W. Fournie
  • David A. Morrison
  • Carlos Azevedo
  • Edilson Matos
  • Per Thebo
  • Michael L. Kent
Original Paper

Abstract

There are numerous species of apicomplexans that infect poikilothermic vertebrates, such as fishes, and possess unique morphological features that provide insight into the evolution of this important phylum of parasites. Here, the relationship of the fish-infecting Calyptospora species to other coccidians was investigated based on DNA sequence analysis. Genetic data from the small subunit ribosomal DNA region of the genome were obtained for three of the five nominal species in the genus Calyptospora. Phylogenetic analyses supported a monophyletic lineage sister to a group composed of mostly Eimeria species. The monophyly of Calyptospora species supports the validity of the family Calyptosporidae, but the sister relationship to Eimeria species might also suggest the Eimeriidae be expanded to encompass Calyptospora. The validity of the family Calyptosporidae has been questioned because it is delineated from the Eimeriidae largely based on life cycle characteristics and sporocyst morphology. In general, Eimeria species have a homoxenous life cycle, whereas the type species of Calyptospora is heteroxenous. In the absence of experimental transmission studies, it may be difficult to demonstrate whether all Calyptospora species are heteroxenous. Other distinct morphological characteristics of Calyptospora such as an incomplete sporocyst suture, an apical opening for sporozoite release, a thin veil surrounding sporocysts supported by sporopodia, and a lack of Stieda and sub-Stieda bodies suggest there may be adequate features to delineate these taxa. Even without life cycle data for all species, the morphology and genetic data provide a means to reliably classify Calyptospora species. Placement in either the Calyptosporidae or Eimeriidae is discussed, along with issues relating to the phylogeny of the genus Goussia.

References

  1. Azevedo C, Matos P, Matos E (1993) Morphological data of Calyptospora spinosa n. sp. (Apicomplexa, Calyptosporidae) parasite of Crenicichla lepidota Heckel, 1840 (Teleostei) from Amazon River. Eur J Protistol 29:171–175CrossRefGoogle Scholar
  2. Barta JR (2001) Molecular approaches for inferring evolutionary relationships among protistan parasites. Vet Parasitol 101:175–186PubMedCrossRefGoogle Scholar
  3. Barta JR, Thompson RCA (2006) What is Cryptosporidium? Reappraising its biology and phylogenetic affinities. Trends Parasitol 22:463–468PubMedCrossRefGoogle Scholar
  4. Beiko RG, Keith JM, Harlow TJ, Ragan MA (2006) Searching for convergence in phylogenetic Markov Chain Monte Carlo. Syst Biol 55:553–565PubMedCrossRefGoogle Scholar
  5. Békési L, Molnár K (1991) Calyptospora tucunarensis n. sp. (Apicomplexa: Sporozoea) from the liver of tucunare Cichla ocellaris in Brazil. Syst Parasitol 18:127–132CrossRefGoogle Scholar
  6. Bonar CJ, Poynton SL, Schulman FY, Rietcheck RL, Garner MM (2006) Hepatic Calyptospora sp. (Apicomplexa) infection in a wild-born, aquarium-held clutch of juvenile arapaima Arapaima gigas (Osteoglossidae). Dis Aquat Organ 70:81–92PubMedCrossRefGoogle Scholar
  7. Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Muller KM, Pande N, Shang Z, Yu N, Gutell RR (2002) The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:2PubMedCrossRefGoogle Scholar
  8. Casal G, Padovan I, Matos E, Padovan P, Matos P, Guimarães A, Azevedo C (2007) Morphological and ultrastructural redescription of Calyptospora serrasalmi Cheung, Nigrelli & Ruggieri, 1986 (Apicomplexa: Calyptosporidae), a parasite found in two new host species of the genus Serrasalmus. Braz J Morphol Sci 24:11–16Google Scholar
  9. Cheung PJ, Nigrelli RF, Ruggieri GD (1986) Calyptospora serrasalmi sp. nov. (Coccidia: Calyptosporidae) from liver of the black piranha, Serrasalmus niger Schomburgk. J Aquat Sci 4:54–57Google Scholar
  10. Dahlgren SS, Gjerde B (2007) Genetic characterisation of six Sarcocystis species from reindeer (Rangifer tarandus tarandus) in Norway based on the small subunit rRNA gene. Vet Parasitol 146:204–213PubMedCrossRefGoogle Scholar
  11. Dahlgren SS, Gjerde B (2009) Sarcocystis in Norwegian roe deer (Capreolus capreolus): molecular and morphological identification of Sarcocystis oviformis n. sp. and Sarcocystis gracilis and their phylogenetic relationship with other Sarcocystis species. Parasitol Res 104:993–1003PubMedCrossRefGoogle Scholar
  12. Dahlgren SS, Gjerde B (2010) Molecular characterization of five Sarcocystis species in red deer (Cervus elaphus), including Sarcocystis hjorti n. sp., reveals that these species are not intermediate host specific. Parasitology 137:815–840PubMedCrossRefGoogle Scholar
  13. Dahlgren SS, Gouveia-Oliveira R, Gjerde B (2008) Phylogenetic relationships between Sarcocystis species from reindeer and other Sarcocystidae deduced from ssu rRNA gene sequences. Vet Parasitol 151:27–35PubMedCrossRefGoogle Scholar
  14. de Albuquerque MC, de Carvalho Brasil‐Sato M (2010) First report of Calyptospora sp. (Apicomplexa, Calyptosporidae) in forage characid fish from the Três Marias Reservoir, São Francisco Basin, Brazil. Eur J Protistol. 46:150‐152Google Scholar
  15. Fournie JW (1985) Biology of Calyptospora funduli (Apicomplexa) from atheriniform fishes. Doctoral dissertation, University of Mississippi, 100 ppGoogle Scholar
  16. Fournie JW, Overstreet RM (1993) Host specificity of Calyptospora funduli (Apicomplexa: Calyptosporidae) in atheriniform fishes. J Parasitol 79:720–727PubMedCrossRefGoogle Scholar
  17. Fournie JW, Overtstreet RM (1983) True intermediate hosts for Eimeria funduli (Apicomplexa) from estuarine fishes. J Protozool 30:672–675Google Scholar
  18. Fournie JW, Hawkins WE, Overstreet RM (1985) Calyptospora empristica n. sp. (Eimeriorina: Calyptosporidae) from the liver of the starhead topminnow, Fundulus notti. J Protozool 32:542–547Google Scholar
  19. Fournie JW, Vogelbein WK, Overstreet RM, Hawkins WE (2000) Life cycle of Calyptospora funduli (Apicomplexa: Calyptosporidae). J Parasitol 86:501–505PubMedGoogle Scholar
  20. Gillespie JJ (2004) Characterizing regions of ambiguous alignment caused by the expansion and contraction of hairpin-stem loops in ribosomal RNA molecules. Mol Phylogenet Evol 33:936–943PubMedCrossRefGoogle Scholar
  21. Gutell RR, Larsen N, Woese CR (1994) Lessons from an evolving rRNA: 16 S and 23 S rRNA structures from a comparative perspective. Microbiol Rev 58:10–26PubMedGoogle Scholar
  22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  23. Hawkins WE, Fournie JW, Overstreet RM (1983) Organization of sporulated oocysts of Eimeria funduli in the gulf killifish, Fundulus grandis. J Parasitol 69:496–503CrossRefGoogle Scholar
  24. Holmdahl OJM, Morrison DA, Ellis JT, Huong LTT (1999) Evolution of ruminant Sarcocystis (Sporozoa) parasites based on small subunit rDNA sequences. Mol Phylogenet Evol 11:27–37PubMedCrossRefGoogle Scholar
  25. Jirků M, Modrý D, Slapeta JR, Koudela B, Lukes J (2002) The phylogeny of Goussia and Choleoeimeria (Apicomplexa; Eimeriorina) and the evolution of excystation structures in coccidia. Protist 153:379–390PubMedCrossRefGoogle Scholar
  26. Jirků M, Bolek MG, Whipps CM, Janovy J, Kent ML, Modry D (2006) A new species of Myxidium (Myxosporea: Myxidiidae), from the western chorus frog, Pseudacris triseriata triseriata, and Blanchard’s cricket frog, Acris crepitans blanchardi (Hylidae) from eastern Nebraska USA: morphology, phylogeny and critical comments on amphibian Myxidium taxonomy. J Parasitol 92:611–619PubMedCrossRefGoogle Scholar
  27. Jirků M, Jirků M, Oborník M, Lukes J, Modry D (2009) Goussia Labbé, 1896 (Apicomplexa, Eimeriorina) in Amphibia: diversity, biology, molecular phylogeny and comments on the status of the genus. Protist 160:123–136PubMedCrossRefGoogle Scholar
  28. Levine ND (1988) The protozoan phylum Apicomplexa, vol I. CRC Press, Boca RatonGoogle Scholar
  29. Lom J, Dyková I (1992) Protozoan parasites of fishes. Developments in aquaculture and fisheries science, 26. Elsevier, Amsterdam, 315 ppGoogle Scholar
  30. Maddison DR, Maddison WP (2000) MacClade: analysis of phylogeny and character evolution. Sinauer Associates, SunderlandGoogle Scholar
  31. Morrison DA (2005) Networks in phylogenetic analysis: new tools for population biology. Int J Parasitol 35:567–582PubMedCrossRefGoogle Scholar
  32. Morrison DA (2006) Phylogenetic analyses of parasites in the new millennium. Adv Parasitol 63:1–124PubMedCrossRefGoogle Scholar
  33. Morrison DA (2009) Evolution of the Apicomplexa: where are we now? Trends Parasitol 25:375–382PubMedCrossRefGoogle Scholar
  34. Morrison DA, Bornstein S, Thebo P, Wernery U, Kinne J, Mattsson JG (2004) The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). Int J Parasitol 34:501–514PubMedCrossRefGoogle Scholar
  35. Overstreet RM, Hawkins WE, Fournie JW (1984) The coccidian genus Calyptospora n.g. and family Calyptosporidae n. fam. (Apicomplexa), with members infecting primarily fishes. J Protozool 31:332–339Google Scholar
  36. Perkins FO, Barta JR, Clopton RE, Peirce MA, Upton SJ (2000) Phylum Apicomplexa. In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the protozoa, 2nd edn. Society of Protozoologists, Lawrence, pp 190–369Google Scholar
  37. Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucl Acids Res 35:7188–7196PubMedCrossRefGoogle Scholar
  38. Rambaut A (2009) FigTree: tree figure drawing tool. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EdinburghGoogle Scholar
  39. Rambaut A, Charleston M (2001) Phylogenetic tree editor. Department of Zoology, University of Oxford, OxfordGoogle Scholar
  40. Rambaut A, Drummond AJ (2007) Tracer: MCMC trace analysis tool. Institute of Evolutionary Biology, University of Edinburgh, EdinburghGoogle Scholar
  41. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  42. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  43. Slapeta J (2008) Taxonomy of the genus Cryptosporidium Tyzzer 1907 (Apicomplexa): revision and checklist—iCRYPTO. Available at http://www.vetsci.usyd.edu.au/staff/JanSlapeta. Accessed on 3 November 2008
  44. Slapeta JR, Kyselova I, Richardson AO, Modry D, Lukês J (2002) Phylogeny and sequence variability of the Sarcocystis singaporensis Zaman and Colley, 1975, 1976 ssrDNA. Parasitol Res 88:810–815PubMedGoogle Scholar
  45. Slapeta JR, Modry D, Votypka J, Jirků M, Lukes J, Koudela B (2003) Evolutionary relationships among cyst-forming coccidia Sarcocystis spp. (Alveolata: Apicomplexa: Coccidea) in endemic African tree vipers and perspective for evolution of heteroxenous life cycle. Mol Phylogenet Evol 27:464–475PubMedCrossRefGoogle Scholar
  46. Solangi MA, Overstreet RM (1980) Biology and pathogenesis of the coccidium Eimeria funduli infecting killifishes. J Parasitol 66:513–526PubMedCrossRefGoogle Scholar
  47. Steinhagen D, Körting W (1990) The role of tubificid oligochaetes in the transmission of Goussia carpelli. J Parasitol 76:104–107PubMedCrossRefGoogle Scholar
  48. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  49. Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlay V, Kent ML (2003) First report of three Kudoa species from eastern Australia: Kudoa thyrsites from Mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from Sweeper (Pempheris ypsilychnus). J Eukaryot Microbiol 50:215–219PubMedCrossRefGoogle Scholar
  50. Work TM, Rameyer RA, Takata G, Kent ML (2003) Protozoal and epitheliocystis-like infections in the introduced bluestripe snapper Lutjanus kasmira in Hawaii. Dis Aquat Organ 57:59–66PubMedCrossRefGoogle Scholar
  51. Wuyts J, De Rijk P, Van de Peer Y, Pison G, Rousseeuw P, De Wachter R (2000) Comparative analysis of more than 3000 sequences reveals the existence of two pseudoknots in area V4 of eukaryotic small subunit ribosomal RNA. Nucl Acids Res 28:4698–4708PubMedCrossRefGoogle Scholar
  52. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31:3406–3415PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Christopher M. Whipps
    • 1
  • John W. Fournie
    • 2
  • David A. Morrison
    • 3
  • Carlos Azevedo
    • 4
    • 5
  • Edilson Matos
    • 6
  • Per Thebo
    • 3
  • Michael L. Kent
    • 7
  1. 1.SUNY‐ESF, State University of New York, College of Environmental Science and Forestry, Environmental and Forest BiologySyracuseUSA
  2. 2.Gulf Ecology Division, National Health and Environmental Effects Research LaboratoryU.S. Environmental Protection AgencyGulf BreezeUSA
  3. 3.Section for Parasitology (SWEPAR), Department of Biomedical Sciences and Veterinary Public HealthSwedish University of Agricultural SciencesUppsalaSweden
  4. 4.Department of Cell Biology, Institute of Biomedical SciencesUniversity of PortoPortoPortugal
  5. 5.Zoology Department, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  6. 6.Laboratório de Pesquisa Carlos AzevedoUniversidade Federal Rural da AmazôniaBelémBrazil
  7. 7.Center for Fish Disease Research, Department of MicrobiologyOregon State UniversityCorvallisUSA

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