Common inheritance of chromosome Ia associated with clonal expansion of Toxoplasma gondii

  1. Asis Khan1,10,
  2. Ulrike Böhme2,10,
  3. Krystyna A. Kelly3,4,10,
  4. Ellen Adlem2,
  5. Karen Brooks2,
  6. Mark Simmonds2,
  7. Karen Mungall2,
  8. Michael A. Quail2,
  9. Claire Arrowsmith2,
  10. Tracey Chillingworth2,
  11. Carol Churcher2,
  12. David Harris2,
  13. Matthew Collins2,
  14. Nigel Fosker2,
  15. Audrey Fraser2,
  16. Zahra Hance2,
  17. Kay Jagels2,
  18. Sharon Moule2,
  19. Lee Murphy2,
  20. Susan O'Neil2,
  21. Marie-Adele Rajandream2,
  22. David Saunders2,
  23. Kathy Seeger2,
  24. Sally Whitehead2,
  25. Thomas Mayr3,
  26. Xuenan Xuan5,
  27. Junichi Watanabe6,
  28. Yutaka Suzuki7,
  29. Hiroyuki Wakaguri7,
  30. Sumio Sugano7,
  31. Chihiro Sugimoto5,
  32. Ian Paulsen8,
  33. Aaron J. Mackey9,
  34. David S. Roos9,
  35. Neil Hall2,8,
  36. Matthew Berriman2,
  37. Bart Barrell2,
  38. L. David Sibley1, and
  39. James W. Ajioka3,11
  1. 1Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, Missouri 63110, USA;
  2. 2The Wellcome Trust Sanger Institute, The Wellcome Trust Genome Campus, Hinxton, CB10 1SA, United Kingdom;
  3. 3Department of Pathology, University of Cambridge, Cambridge, CB2 1QP, United Kingdom;
  4. 4MRC Biostatistics Unit, Institute of Public Health, Cambridge, CB2 2SR, United Kingdom;
  5. 5National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, 080-8555, Japan;
  6. 6Department of Parasitology, Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo, 108-8639, Japan;
  7. 7Department of Medical Genomics, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan;
  8. 8The Institute for Genomic Research, Rockville, Maryland 20850, USA;
  9. 9Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA

    1. ↵10 These authors contributed equally to this work.

    Abstract

    Toxoplasma gondii is a globally distributed protozoan parasite that can infect virtually all warm-blooded animals and humans. Despite the existence of a sexual phase in the life cycle, T. gondii has an unusual population structure dominated by three clonal lineages that predominate in North America and Europe, (Types I, II, and III). These lineages were founded by common ancestors ~10,000 yr ago. The recent origin and widespread distribution of the clonal lineages is attributed to the circumvention of the sexual cycle by a new mode of transmission—asexual transmission between intermediate hosts. Asexual transmission appears to be multigenic and although the specific genes mediating this trait are unknown, it is predicted that all members of the clonal lineages should share the same alleles. Genetic mapping studies suggested that chromosome Ia was unusually monomorphic compared with the rest of the genome. To investigate this further, we sequenced chromosome Ia and chromosome Ib in the Type I strain, RH, and the Type II strain, ME49. Comparative genome analyses of the two chromosomal sequences revealed that the same copy of chromosome Ia was inherited in each lineage, whereas chromosome Ib maintained the same high frequency of between-strain polymorphism as the rest of the genome. Sampling of chromosome Ia sequence in seven additional representative strains from the three clonal lineages supports a monomorphic inheritance, which is unique within the genome. Taken together, our observations implicate a specific combination of alleles on chromosome Ia in the recent origin and widespread success of the clonal lineages of T. gondii.

    Footnotes

    • ↵11 Corresponding author.

      ↵11 E-mail ja131{at}cam.ac.uk; fax 44-1223-333346.

    • Article published online before print. Article and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.5318106.

    • Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to EMBL under accession nos. AM055942 and AM055943. Accession numbers for full-length cDNAs associated with chromosomes Ia and Ib are AK223637–AK223774.

      • Received March 21, 2006.
      • Accepted June 6, 2006.
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    1. Published in Advance August 10, 2006, doi: 10.1101/gr.5318106 Genome Res. 16: 1119-1125 Copyright © 2006, Cold Spring Harbor Laboratory Press

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