Whole genome sequencing of a natural recombinant Toxoplasma gondii strain reveals chromosome sorting and local allelic variants

Genome Biology

Volumn 10, Issue 5, 2009, Pages

  Bontell, Irene Lindström ^a,f   Hall, Neil ^b   Ashelford, Kevin E ^b   Dubey, J P ^c   Boyle, Jon P ^d   Lindh, Johan ^e   Smith, Judith E ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE ANTIGEN; PROTOZOAL PROTEIN; RHOPTRY; UNCLASSIFIED DRUG;

ALLELE; ANIMAL TISSUE; APICOPLAST; ARTICLE; CHROMOSOME; GENE MAPPING; GENE SEQUENCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; TOXOPLASMA GONDII; ANIMAL; CLASSIFICATION; GENETICS; GENOME; ISOLATION AND PURIFICATION; NORTH AMERICA; PARASITOLOGY; TOXOPLASMA; TOXOPLASMOSIS; UGANDA;

MUS; PROTOZOA; TOXOPLASMA GONDII;

ALLELES; ANIMALS; GENOME, PROTOZOAN; HUMANS; NORTH AMERICA; POLYMORPHISM, SINGLE NUCLEOTIDE; RECOMBINATION, GENETIC; TOXOPLASMA; TOXOPLASMOSIS; UGANDA;

EID: 67650735559     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-5-r53     Document Type: Article

References (47)

1. Smith JE Tracking transmission of the zoonosis Toxoplasma gondii. Adv Parasitol 2009, 68:139-159. 19289193
2. Grigg ME Suzuki Y Sexual recombination and clonal evolution of virulence in Toxoplasma. Microbes Infect 2003, 5:685-690. 12787745
3. Khan A Taylor S Su C Mackey AJ Boyle J Cole R Glover D Tang K Paulsen IT Berriman M Boothroyd JC Pfeffercorn ER Dubey JP Ajioka JW Roos DS Wooton JC Sibley LD Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii. Nucleic Acids Res 2005, 33:2980-2992. 1137028 15911631
4. Pfefferkorn ER Kasper LH Toxoplasma gondii: Genetic crosses reveal phenotypic suppression of hydroxyurea resistance by fluorodeoxyuridine resistance. Exp Parasitol 1983, 55:207-218. 6219892
5. Pfefferkorn LC Pfefferkorn ER Toxoplasma gondii: Genetic recombination between drug resistant mutants. Exp Parasitol 1980, 50:305-316. 6448752
6. Sibley LD LeBlanc AJ Pfefferkorn ER Boothroyd JC Generation of a restriction fragment length polymorphism linkage map for Toxoplasma gondii. Genetics 1992, 132:1003-1015. 1205223 1360931
7. Grigg ME Bonnefoy S Hehl AB Suzuki Y Boothroyd JC Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 2001, 294:161-165. 11588262
8. Khan A Fux B Su C Dubey JP Darde ML Ajioka JW Rosenthal BM Sibley LD Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Proc Natl Acad Sci USA 2007, 104:14872-14877. 1965483 17804804
9. Pena HF Gennari SM Dubey JP Su C Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Int J Parasitol 2007, 38:561-569. 17963770
10. Ajzenberg D Banuls AL Su C Dumetre A Demar M Carme B Darde ML Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int J Parasitol 2004, 34:1185-1196. 15380690
11. Dubey JP Cortes-Vecino JA Vargas-Duarte JJ Sundar N Velmurugan GV Bandini LM Polo LJ Zambrano L Mora LE Kwok OC Smith T Su C Prevalence of Toxoplasma gondii in dogs from Colombia, South America and genetic characterization of T. gondii isolates. Vet Parasitol 2007, 145:45-50. 17257761
12. Lehmann T Marcet PL Graham DH Dahl ER Dubey JP Globalization and the population structure of Toxoplasma gondii. Proc Natl Acad Sci USA 2006, 103:11423-11428. 1544101 16849431
13. Boyle JP Rajasekar B Saeij JP Ajioka JW Berriman M Paulsen I Roos DS Sibley LD White MW Boothroyd JC Just one cross appears capable of dramatically altering the population biology of a eukaryotic pathogen like Toxoplasma gondii. Proc Natl Acad Sci USA 2006, 103:10514-10519. 1502489 16801557
14. ToxoDB http://toxodb.org/toxo/
15. Gajria B Bahl A Brestelli J Dommer J Fischer S Gao X Heiges M Iodice J Kissinger JC Mackey AJ Pinney DF Roos DS Stoeckert CJ Wang H Brunk BP ToxoDB: An integrated Toxoplasma gondii database resource. Nucleic Acids Res 2008, 36: Database D553-556. 2238934 18003657
16. Khan A Bohme U Kelly KA Adlem E Brooks K Simmonds M Mungall K Quail MA Arrowsmith C Chillingworth T Churcher C Harris D Collins M Fosker N Fraser A Hance Z Jagels K Moule S Murphy L O'Neil S Rajandream MA Saunders D Seeger K Whitehead S Mayr T Xuan X Watanabe J Suzuki Y Wakaguri H Sugano S et al Common inheritance of chromosome Ia associated with clonal expansion of Toxoplasma gondii. Genome Res 2006, 16:1119-1125. 1557770 16902086
17. Sibley LD Ajioka JW Population Structure of Toxoplasma gondii: Clonal expansion driven by infrequent recombination and selective sweeps. Annu Rev Microbiol 2008, 62:329-351. 18544039
18. Velmurugan GV Dubey JP Su C Genotyping studies of Toxoplasma gondii isolates from Africa revealed that the archetypal clonal lineages predominate as in North America and Europe. Vet Parasitol 2008, 155:314-318. 18583059
19. Lindstrom I Sundar N Lindh J Kironde F Kabasa JD Kwok OC Dubey JP Smith JE Isolation and genotyping of Toxoplasma gondii from Ugandan chickens reveals frequent multiple infections. Parasitology 2008, 135:39-45. 17892617
20. Swaminathan K Varala K Hudson ME Global repeat discovery and estimation of genomic copy number in a large, complex genome using a high-throughput 454 sequence survey. BMC Genomics 2007, 8:132. 1894642 17524145
21. Fichera ME Roos DS A plastid organelle as a drug target in apicomplexan parasites. Nature 1997, 390:407-409. 9389481
22. Kohler S Delwiche CF Denny PW Tilney LG Webster P Wilson RJ Palmer JD Roos DS A plastid of probable green algal origin in Apicomplexan parasites. Science 1997, 275:1485-1489. 9045615
23. Matsuzaki M Kikuchi T Kita K Kojima S Kuroiwa T Large amounts of apicoplast nucleoid DNA and its segregation in Toxoplasma gondii. Protoplasma 2001, 218:180-191. 11770434
24. Ferguson DJ Henriquez FL Kirisits MJ Muench SP Prigge ST Rice DW Roberts CW McLeod RL Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host. Eukaryot Cell 2005, 4:814-826. 1087807 15821140
25. Yang Z Computational Molecular Evolution Oxford: Oxford University Press 2006.
26. Su C Evans D Cole RH Kissinger JC Ajioka JW Sibley LD Recent expansion of Toxoplasma through enhanced oral transmission. Science 2003, 299:414-416. 12532022
27. Morrison DA How old are the extant lineages of Toxoplasma gondii? Parassitologia 2005, 47:205-214. 16252475
28. Toxoplasma Genome Map http://toxomap.wustl.edu/
29. Innes EA Toxoplasmosis: Comparative species susceptibility and host immune response. Comp Immunol Microbiol Infect Dis 1997, 20:131-138. 9208198
30. Frenkel JK Pathophysiology of toxoplasmosis. Parasitol Today 1988, 4:273-278. 15463000
31. Araujo F Slifer T Kim S Chronic infection with Toxoplasma gondii does not prevent acute disease or colonization of the brain with tissue cysts following reinfection with different strains of the parasite. J Parasitol 1997, 83:521-522. 9194838
32. Dao A Fortier B Soete M Plenat F Dubremetz JF Successful reinfection of chronically infected mice by a different Toxoplasma gondii genotype. Int J Parasitol 2001, 31:63-65. 11165272
33. Dzitko K Staczek P Gatkowska J Dlugonska H Toxoplasma gondii: Serological recognition of reinfection. Exp Parasitol 2006, 112:134-137. 16289467
34. Aspinall TV Guy EC Roberts KE Joynson DH Hyde JE Sims PF Molecular evidence for multiple Toxoplasma gondii infections in individual patients in England and Wales: Public health implications. Int J Parasitol 2003, 33:97-103. 12547351
35. Ferreira Ade M Vitor RW Gazzinelli RT Melo MN Genetic analysis of natural recombinant Brazilian Toxoplasma gondii strains by multilocus PCR-RFLP. Infect Genet Evol 2006, 6:22-31. 16376837
36. Dubey JP Sundar N Pineda N Kyvsgaard NC Luna LA Rimbaud E Oliveira JB Kwok OC Qi Y Su C Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Nicaragua, Central America. Vet Parasitol 2006, 142:47-53. 16876324
37. Beck HP Blake D Darde ML Felger I Pedraza-Diaz S Regidor-Cerrillo J Gomez-Bautista M Ortega-Mora LM Putignani L Shiels B Tait A Weir W Molecular approaches to diversity of populations of apicomplexan parasites. Int J Parasitol 2009, 39:175-189. 18983997
38. Su C Howe DK Dubey JP Ajioka JW Sibley LD Identification of quantitative trait loci controlling acute virulence in Toxoplasma gondii. Proc Natl Acad Sci USA 2002, 99:10753-10758. 125035 12149482
39. Bromham L Penny D The modern molecular clock. Nat Rev Genet 2003, 4:216-224. 12610526
40. Zuckerkandl E Pauling L Molecules as documents of evolutionary history. J Theor Biol 1965, 8:357-366. 5876245
41. Saeij JP Boyle JP Coller S Taylor S Sibley LD Brooke-Powell ET Ajioka JW Boothroyd JC Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 2006, 314:1780-1783. 2646183 17170306
42. Taylor S Barragan A Su C Fux B Fentress SJ Tang K Beatty WL Hajj HE Jerome M Behnke MS White M Wootton JC Sibley LD A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 2006, 314:1776-1780. 17170305
43. Bradley PJ Sibley LD Rhoptries: An arsenal of secreted virulence factors. Curr Opin Microbiol 2007, 10:582-587. 2682365 17997128
44. Craver MP Knoll LJ Increased efficiency of homologous recombination in Toxoplasma gondii dense granule protein 3 demonstrates that GRA3 is not necessary in cell culture but does contribute to virulence. Mol Biochem Parasitol 2007, 153:149-157. 17418907
45. Jung C Lee CY Grigg ME The SRS superfamily of Toxoplasma surface proteins. Int J Parasitol 2004, 34:285 296. 15003490
46. Dubey JP Re-examination of resistance of Toxoplasma gondii tachyzoites and bradyzoites to pepsin and trypsin digestion. Parasitology 1998, 116:43-50. 9481773
47. Homan WL Vercammen M De Braekeleer J Verschueren H Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Int J Parasitol 2000, 30:69-75. 10675747