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Molecular phylogenetics of eimeriid coccidia (Eimeriidae, Eimeriorina, Apicomplexa, Alveolata): A preliminary multi-gene and multi-genome approach

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Abstract

Coccidia possess three distinct genomes: nuclear, mitochondrial, and plastid. Sequences from five genes located on these three genomes were used to reconstruct the phylogenetic relationships of members of the phylum Apicomplexa: 18S rDNA sequences from the nuclear (nu) genome, partial cytochrome c oxidase subunit I sequences from the mitochondrial (mt) genome, and partial 16S and 23S rDNA sequences and RNA polymerase B sequences from plastid (pl) genomes. Maximum parsimony, maximum likelihood, and Bayesian inference were used in conjunction with nuclear substitution models generated from data subsets in the analyses. Major groups within the Apicomplexa were well supported with the mitochondrial, nuclear, and a combination of mitochondrial, nuclear and concatenated plastid gene sequences. However, the genus Eimeria was paraphyletic in phylogenetic trees based on the nuclear gene. Analyses using the individual genes (18S rDNA and cytochrome c oxidase subunit I) resolved the various apicomplexan groups with high Bayesian posterior probabilities. The multi-gene, multi-genome analyses based on concatenated nu 18S rDNA, pl 16S, pl 23S, pl rPoB, pl rPoB1, and mt COI sequences appeared useful in resolving phylogenetic relationships within the phylum Apicomplexa. Genus-level relationships, or higher, appear best supported by 18S rDNA analyses, and species-level analyses are best investigated using mt COI sequences; for parasites for which both loci are available, nuclear 18S rDNA sequences combined with mitochondrial COI sequences provide a compact and informative molecular dataset for inferring the evolutionary relationships taxa in the Apicomplexa.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool (BLAST). J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New York

    Book  Google Scholar 

  • Barta JR (1997) Investigating phylogenetic relationships within the phylum Apicomplexa using sequence data: the search for homology. Methods 13:81–88

    Article  CAS  PubMed  Google Scholar 

  • Barta JR (2001) Molecular approaches for inferring evolutionary relationships among protistan parasites. Vet Parasitol 101:175–86

    Article  CAS  PubMed  Google Scholar 

  • Barta JR, Martin DS, Carreno RA, Siddall ME, Profous-Juchelka H, Hozza M, Powles MA, Sundermann C (2001) Molecular phylogeny of the other tissue coccidia: Lankesterella and Caryospora. J Parasitol 87:121–127

    Article  CAS  PubMed  Google Scholar 

  • Barta JR, Martin DS, Liberator DA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271

    Article  CAS  PubMed  Google Scholar 

  • Barta JR, Schrenzel MD, Carreno RA, Rideout BA (2005) The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals. J Parasitol 91:726–727

    Article  CAS  PubMed  Google Scholar 

  • Bhoora R, Franssen L, Oosthuizen MC, Guthrie AJ, Zweygarth E, Penzhorn BL, Jongejan F, Collins NE (2009) Sequence heterogeneity in the 18S rDNA gene18S rDNA within Theileria equi and Babesia caballi from horses in South Africa. Vet Parasitol 159:112–120

    Article  CAS  PubMed  Google Scholar 

  • Blanchard JL, Hicks JS (1999) The non-photosynthetic plastid in malarial parasites and other apicomplexans is derived from outside the green plastid lineage. J Eukaryot Microbiol 46:367–375

    Article  CAS  PubMed  Google Scholar 

  • Cai X, Fuller AL, McDougald LR, Zhu G (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39–46

    Article  CAS  PubMed  Google Scholar 

  • Carranza S, Giribet G, Ribera C, Baguñà J, Riutort M (1996) Evidence that two types of 18S rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Mol Biol Evol 13:824–832

    Article  CAS  PubMed  Google Scholar 

  • Carreno RA, Barta JR (1999) An eimeriid origin of isosporoid coccidia with Stieda bodies as shown by phylogenetic analysis of small subunit ribosomal RNA gene sequences. J Parasitol 85:77–83

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1983) A six-kingdom classified and unified phylogeny. In: Schwemmler W, Schenk HEA (eds) Endocytobiology II. Intracellular space as oligogenetic ecosystem. De Gruyter, Berlin, pp 1027–1034

    Google Scholar 

  • Cavalier-Smith T (1993) Kingdom of protozoa and its 18 phyla. Microbiol Rev 57:953–994

    PubMed Central  CAS  PubMed  Google Scholar 

  • de Queiroz A, Donoghue MJ, Kim J (1995) Separate versus combined analysis of phylogenetic evidence. Ann Rev Ecol Syst 26:657–681

    Article  Google Scholar 

  • Eernisse DJ, Kluge AG (1993) Taxonomic congruence versus total evidence and amniote phylogeny inferred from fossils, molecules, and morphology. Mol Biol Evol 10:1170–1195

    CAS  PubMed  Google Scholar 

  • El-Sherry S, Ogedengbe ME, Hafeez MA, Barta JR (2013) Divergent nuclear 18S rDNA paralogs in a turkey coccidium, Eimeria meleagrimitis, complicate molecular systematics and identification. Int J Parasitol 43:679–85

    Article  CAS  PubMed  Google Scholar 

  • Escalante AA, Ayala FJ (1994) Phylogeny of the malarial genus Plasmodium, derived from rDNA gene sequences. Proc Natl Acad Sci USA 91:11373–11377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferguson DJ, Henriquez FL, Kirisits MJ, Muench SP, Prigge ST, Rice DW, Roberts CW, McLeod RL (2005) Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host. Eukaryot Cell 4:814–826

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gadagkar SR, Rosenberg MS, Kumar S (2005) Inferring species phylogenies from multiple genes: concatenated sequence tree versus consensus gene tree. J Exp Zool B Mol Dev Evol 304:64–74

    Article  PubMed  Google Scholar 

  • Gagnon S, Bourbeau D, Levesque RC (1996) Secondary structures and features of the 18S, 5.8S and 26S ribosomal RNAs from the apicomplexan parasite Toxoplasma gondii. Gene 173:129–135

    Article  CAS  PubMed  Google Scholar 

  • Hagner SC, Misof B, Maier WA, Kampen H (2007) Bayesian analysis of new and old malaria parasite DNA sequence data demonstrates the need for more phylogenetic signal to clarify the descent of Plasmodium falciparum. Parasitol Res 101:493–503

    Article  CAS  PubMed  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, de Waard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 10:14812–14817

    Article  Google Scholar 

  • Hikosaka K, Watanabe Y TN, Kita K, Kishine H, Arisue N, Palacpac NM, Kawazu S, Sawai H, Horii T, Igarashi I, Tanabe K (2010) Divergence of the mitochondrial genome structure in the apicomplexan parasites, Babesia and Theileria. Mol Biol Evol 27:1107–1116

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jirků M, Jirků M, Oborník M, Lukeš J, Modrý D (2009) A model for taxonomic work on homoxenous coccidia: redescription, host specificity, and molecular phylogeny of Eimeria ranae Dobell, 1909, with a review of anuran-host Eimeria (Apicomplexa: Eimeriorina). J Eukaryot Microbiol 56:39–51

    Article  PubMed  Google Scholar 

  • 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 153:379–390

    Article  PubMed  Google Scholar 

  • Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64

    Article  CAS  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed Central  PubMed  Google Scholar 

  • Kedzierski L, Escalante AA, Isea R, Black CG, Barnwell JW, Coppel RL (2002) Phylogenetic analysis of the genus Plasmodium based on the gene encoding adenylosuccinate lyase. Infect Genet Evol 1:297–301

    Article  CAS  PubMed  Google Scholar 

  • Lang-Unash N, Reith ME, Munholland J, Barta JR (1998) Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int J Parasitol 28:1743–1754

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lau AO, McElwain TF, Brayton KA, Knowles DP, Roalson EH (2009) Babesia bovis: a comprehensive phylogenetic analysis of plastid-encoded genes supports green algal origin of apicoplasts. Exp Parasitol 123:236–243

    Article  CAS  PubMed  Google Scholar 

  • Leander BS, Harper JT, Keeling PJ (2003) Molecular phylogeny and surface morphology of marine aseptate Gregarines (Apicomplexa): Selenidium spp. and Lecudina spp. J Parasitol 89:1191–1205

    Article  CAS  PubMed  Google Scholar 

  • Li J, Gutell RR, Damberger SH, Wirtz RA, Kissinger JC, Rogers MJ, Sattabongkot J, McCutchan TF (1997) Regulation and trafficking of three distinct 18S ribosomal RNAs during development of the malaria parasite. J Mol Biol 269:203–213

    Article  CAS  PubMed  Google Scholar 

  • Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol Phylogenet Evol 47:261–273

    Article  CAS  PubMed  Google Scholar 

  • McCutchan TF, Li J, McConkey GA, Rogers MJ, Waters AP (1995) The cytoplasmic ribosomal RNAs of Plasmodium spp. Parasitol Today 11:134–138

    Article  CAS  PubMed  Google Scholar 

  • Monteiro RM, Richtzenhain LJ, Pena HF, Souza SL, Funada MR, Gennari SM, Dubey JP, Sreekumar C, Keid LB, Soares RM (2007) Molecular phylogenetic analysis in Hammondia-like organisms based on partial Hsp70 coding sequences. Parasitology 134:1195–1203

    Article  CAS  PubMed  Google Scholar 

  • Morrison DA (2008) Prospects for elucidating the phylogeny of the Apicomplexa. Parasite 15:191–193

    Article  CAS  PubMed  Google Scholar 

  • Morrison DA (2009) Evolution of the Apicomplexa: where are we now? Trends Parasitol 25:375–382

    Article  PubMed  Google Scholar 

  • 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 34:501–514

    Article  CAS  PubMed  Google Scholar 

  • Mugridge NB, Morrison DA, Heckeroth AR, Johnson AM, Tenter AM (1999) Phylogenetic analysis based on full-length large subunit ribosomal RNA gene sequence comparison reveals that Neospora caninum is more closely related to Hammondia heydorni than to Toxoplasma gondii. Int J Parasitol 29:1545–1556

    Article  CAS  PubMed  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  • Ogedengbe JD, Hanner RH, Barta JR (2011) DNA barcoding identifies Eimeria species and contributes to the phylogenetics of coccidian parasites (Eimeriorina, Apicomplexa, Alveolata). Int J Parasitol 418:843–850

    Article  Google Scholar 

  • Omori S, Sato Y, Isobe T, Yukawa M, Murata K (2007) Complete nucleotide sequences of the mitochondrial genomes of two avian malaria protozoa, Plasmodium gallinaceum and Plasmodium juxtanucleare. Parasitol Res 100:661–664

    Article  PubMed  Google Scholar 

  • Outlaw DC, Ricklefs RE (2010) Comparative gene evolution in haemosporidian (Apicomplexa) parasites of birds and mammals. Mol Biol Evol 27:537–542

    Article  CAS  PubMed  Google Scholar 

  • Perkins SL (2008) Molecular systematics of the three mitochondrial protein-coding genes of malaria parasites: corroborative and new evidence for the origins of human malaria. Mitochondrial DNA 19:471–478

    Article  CAS  PubMed  Google Scholar 

  • Perkins SL, Sarkar IN, Carter R (2007) The phylogeny of rodent malaria parasites: simultaneous analysis across three genomes. Infect Genet Evol 7:74–83

    Article  CAS  PubMed  Google Scholar 

  • Power ML, Richter C, Emery S, Hufschmid J, Gillings MR (2009) Eimeria trichosuri: phylogenetic position of a marsupial coccidium, based on 18S rDNA sequences. Exp Parasitol 122:165–168

    Article  CAS  PubMed  Google Scholar 

  • Putignani L, Tait A, Smith HV, Horner D, Tovar J, Tetley L, Wastling JM (2004) Characterization of a mitochondrion-like organelle in Cryptosporidium parvum. Parasitology 129:1–18

    Article  CAS  PubMed  Google Scholar 

  • Rathore D, Wahl AM, Sullivan M, McCutchan TF (2001) A phylogenetic comparison of gene trees constructed from plastid, mitochondrial and genomic DNA of Plasmodium species. Mol Biochem Parasitol 114:89–94

    Article  CAS  PubMed  Google Scholar 

  • Reid WM, Long PL (1979) A diagnostic chart for nine species of fowl coccidia. Research Report (University of Georgia College of Agriculture Experimental Stations) 335:1–24

    Google Scholar 

  • Samarasinghe B, Johnson J, Ryan U (2008) Phylogenetic analysis of Cystoisospora species at the rRNA ITS1 locus and development of a PCR-RFLP assay. Exp Parasitol 118:592–595

    Article  CAS  PubMed  Google Scholar 

  • Saxena AK, Wu Y, Garboczi DN (2007) Plasmodium p25 and p28 surface proteins: potential transmission-blocking vaccines. Eukaryot Cell 6:1260–1265

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schrenzel MD, Maalouf GA, Gaffney PM, Tokarz D, Keener LL, McClure D, Griffey S, McAloose D, Rideout BA (2005) Molecular characterization of isosporoid coccidia (Isospora and Atoxoplasma spp.) in passerine birds. J Parasitol 91:635–647

    Article  CAS  PubMed  Google Scholar 

  • Schwarz RH, Ryan S, Schwarz RS, Jenkins MC, Klopp S, Miska KB (2009) Genomic analysis of Eimeria spp. populations in relation to performance levels of broiler chicken farms in Arkansas and North Carolina, U.S.A. J Parasitol 95:871–880

    Article  CAS  PubMed  Google Scholar 

  • Siddall ME, Reece KS, Graves JE, Burreson EM (1997) ‘Total evidence” refutes the inclusion of Perkinsus species in the phylum Apicomplexa. Parasitology 115:165–176

    Article  PubMed  Google Scholar 

  • Slapeta JR, Modrý D, Votýpka 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 27:464–475

    Article  CAS  PubMed  Google Scholar 

  • Suchard MA, Kitchen CMR, Sinsheimer JS, Weiss RE (2003) Hierarchical phylogenetic models for analyzing multipartite sequence data. Syst Biol 52:649–664

    Article  PubMed  Google Scholar 

  • Swofford DL (2003) PAUP: Phylogenetic Analysis Using Parsimony (and other methods). Version 4.10b. Sinauer Associates, Sunderland

    Google Scholar 

  • Tenter AM, Barta JR, Beveridge I, Duszynski DW, Mehlhorn H, Morrison DA, Thompson RCA, Conrad PA (2002) The conceptual basis for a new classification of the coccidia. Int J Parasitol 32:595–616

    Article  PubMed  Google Scholar 

  • Vrba V, Poplstein M, Pakandl M (2011) The discovery of the two types of small subunit ribosomal RNA gene in Eimeria mitis contests the existence of E. mivati as an independent species. Vet Parasitol 183:47–53

    Article  CAS  PubMed  Google Scholar 

  • Votýpka J, Hypsa V, Jirků M, Flegr J, Vávra J, Lukes J (1998) Molecular phylogenetic relatedness of Frenkelia spp. (Protozoa, Apicomplexa) to Sarcocystis falcatula Stiles 1893: is the genus Sarcocystis paraphyletic? J Eukaryot Microbiol 45:137–141

    Article  PubMed  Google Scholar 

  • Waller RF, McFadden GI (2005) The apicoplast: a review of the derived plastid of apicomplexan parasites. Curr Issues Mol Biol 7:57–79

    PubMed  Google Scholar 

  • Whipps CM, Fournie JW, Morrison DA, Azevedo C, Matos E, Thebo P, Kent ML (2012) Phylogeny of fish-infecting Calyptospora species (Apicomplexa: Eimeriorina). Parasitol Res 111:1331–1342

    Article  PubMed  Google Scholar 

  • Wilson RJM, Williamson DH (1997) Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev 61:1–16

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang Z (1996) Maximum-likelihood models for combined analyses of multiple sequence data. J Mol Evol 42:587–596

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Duszynski DW (2001) Phylogenetic relationships among rodent Eimeria species determined by plastid ORF470 and nuclear 18S rDNA sequences. Int J Parasitol 31:715–719

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Duszynski DW, Loker ES (2001) Phylogenetic position of Eimeria antrozoi, a bat coccidium (Apicomplexa: Eimeriidae) and its relationship to morphologically similar Eimeria spp. from bats and rodents based on nuclear 18S rDNA and plastid 23S rDNA sequences. J Parasitol 87:1120–1123

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The Natural Sciences and Engineering Research Council of Canada (NSERC) and the Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA) are acknowledged for funding this research through grants to JRB. Julie Cobean is thanked for her technical support during this project.

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  1. Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Joseph D. Ogedengbe, Mosun E. Ogedengbe, Mian A. Hafeez & John R. Barta

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  1. Joseph D. Ogedengbe
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  2. Mosun E. Ogedengbe
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  3. Mian A. Hafeez
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  4. John R. Barta
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Ogedengbe, J.D., Ogedengbe, M.E., Hafeez, M.A. et al. Molecular phylogenetics of eimeriid coccidia (Eimeriidae, Eimeriorina, Apicomplexa, Alveolata): A preliminary multi-gene and multi-genome approach. Parasitol Res 114, 4149–4160 (2015). https://doi.org/10.1007/s00436-015-4646-1

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