Self-mating in the definitive host potentiates clonal outbreaks of the apicomplexan parasites Sarcocystis neurona and Toxoplasma gondii

PLoS Genetics

Volumn 6, Issue 12, 2010, Pages 1-13

  Wendte, Jered M ^a,b,c   Miller, Melissa A ^d   Lambourn, Dyanna M ^e   Magargal, Spencer L ^a   Jessup, David A ^d   Grigg, Michael E ^a,b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d Marine Wildlife Veterinary Care and Research Center   (United States)

^e Department of Fish and Wildlife ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APICOMPLEXA; ARTICLE; CLONE; EPIDEMIC; EQUINE PROTOZOAL MYELOENCEPHALITIS; GENOTYPE; GEOGRAPHIC DISTRIBUTION; MATING; NONHUMAN; OOCYTE; PARASITE ISOLATION; PARASITE VIRULENCE; POPULATION GENETIC STRUCTURE; PROGENY; SARCOCYSTIS NEURONA; SEXUAL BEHAVIOR; SPOROCYST; TOXOPLASMA GONDII; TOXOPLASMOSIS; ANIMAL; ANIMAL DISEASE; BRAZIL; CARNIVORA; CLASSIFICATION; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; HUMAN; MOLECULAR GENETICS; OOCYST; PARASITOLOGY; PHYSIOLOGY; SARCOCYSTIS; SARCOCYSTOSIS; SELF FERTILIZATION; TOXOPLASMA;

COCCIDIA; ENHYDRA LUTRIS NEREIS; SARCOCYSTIS NEURONA; TOXOPLASMA GONDII;

ANIMALS; BRAZIL; DISEASE OUTBREAKS; GENOTYPE; HOST-PARASITE INTERACTIONS; HUMANS; MOLECULAR SEQUENCE DATA; OOCYSTS; OTTERS; RECOMBINATION, GENETIC; SARCOCYSTIS; SARCOCYSTOSIS; SELF-FERTILIZATION; TOXOPLASMA; TOXOPLASMOSIS;

EID: 78650701465     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001261     Document Type: Article

References (85)

1. Li W, Raoult D, Fournier PE (2009) Bacterial strain typing in the genomic era. FEMS Microbiol Rev 33: 892-916.
2. Feil EJ, Spratt BG (2001) Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol 55: 561-590.
3. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, et al. (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125.
4. Powers C, DeFilippis V, Malouli D, Fruh K (2008) Cytomegalovirus immune evasion. Curr Top Microbiol Immunol 325: 333-359.
5. Aires-de-Sousa M, Correia B, de Lencastre H (2008) Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol 46: 2912-2917.
6. Amorim ML, Faria NA, Oliveira DC, Vasconcelos C, Cabeda JC, et al. (2007) Changes in the clonal nature and antibiotic resistance profiles of methicillinresistant Staphylococcus aureus isolates associated with spread of the EMRSA-15 clone in a tertiary care Portuguese hospital. J Clin Microbiol 45: 2881-2888.
7. Fraser C, Hanage WP, Spratt BG (2005) Neutral microepidemic evolution of bacterial pathogens. Proc Natl Acad Sci U S A 102: 1968-1973.
8. Ogura Y, Ooka T, Iguchi A, Toh H, Asadulghani M, et al. (2009) Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci U S A 106: 17939-17944.
9. Reid SD, Herbelin CJ, Bumbaugh AC, Selander RK, Whittam TS (2000) Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406: 64-67.
10. Akopyants NS, Kimblin N, Secundino N, Patrick R, Peters N, et al. (2009) Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324: 265-268.
11. Byrnes EJ, III, Li W, Lewit Y, Ma H, Voelz K, et al. (2010) Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog 6: e1000850. doi:10.1371/journal.ppat.1000850.
12. Fraser JA, Giles SS, Wenink EC, Geunes-Boyer SG, Wright JR, et al. (2005) Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437: 1360-1364.
13. Boyle JP, Rajasekar B, Saeij JP, Ajioka JW, Berriman M, et al. (2006) Just one cross appears capable of dramatically altering the population biology of a eukaryotic pathogen like Toxoplasma gondii. Proc Natl Acad Sci U S A 103: 10514-10519.
14. Grigg ME, Bonnefoy S, Hehl AB, Suzuki Y, Boothroyd JC (2001) Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 294: 161-165.
15. Gaunt MW, Yeo M, Frame IA, Stothard JR, Carrasco HJ, et al. (2003) Mechanism of genetic exchange in American trypanosomes. Nature 421: 936-939.
16. Jenni L, Marti S, Schweizer J, Betschart B, Le Page RW, et al. (1986) Hybrid formation between African trypanosomes during cyclical transmission. Nature 322: 173-175.
17. Aly AS, Vaughan AM, Kappe SH (2009) Malaria parasite development in the mosquito and infection of the mammalian host. Annu Rev Microbiol 63: 195-221.
18. Howe DK, Sibley LD (1995) Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis 172: 1561-1566.
19. Su C, Evans D, Cole RH, Kissinger JC, Ajioka JW, et al. (2003) Recent expansion of Toxoplasma through enhanced oral transmission. Science 299: 414-416.
20. Grigg ME, Sundar N (2009) Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. Int J Parasitol 39: 925-933.
21. Sibley LD, Ajioka JW (2008) Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu Rev Microbiol 62: 329-351.
22. Asmundsson IM, Dubey JP, Rosenthal BM (2006) A genetically diverse but distinct North American population of Sarcocystis neurona includes an overrepresented clone described by 12 microsatellite alleles. Infect Genet Evol 6: 352-360.
23. Rejmanek D, Miller MA, Grigg ME, Crosbie PR, Conrad PA (2010) Molecular characterization of Sarcocystis neurona strains from opossums (Didelphis virginiana) and intermediate hosts from Central California. Vet Parasitol 170: 20-29.
24. Sundar N, Asmundsson IM, Thomas NJ, Samuel MD, Dubey JP, et al. (2008) Modest genetic differentiation among North American populations of Sarcocystis neurona may reflect expansion in its geographic range. Vet Parasitol 152: 8-15.
25. Wendte JM, Miller MA, Nandra AK, Peat SM, Crosbie PR, et al. (2010) Limited genetic diversity among Sarcocystis neurona strains infecting southern sea otters precludes distinction between marine and terrestrial isolates. Vet Parasitol 169: 37-44.
26. Tibayrenc M, Ayala FJ (2002) The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol 18: 405-410.
27. Dubey JP (2009) History of the discovery of the life cycle of Toxoplasma gondii. Int J Parasitol 39: 877-882.
28. Hide G, Morley EK, Hughes JM, Gerwash O, Elmahaishi MS, et al. (2009) Evidence for high levels of vertical transmission in Toxoplasma gondii. Parasitology 136: 1877-1885.
29. Innes EA, Bartley PM, Buxton D, Katzer F (2009) Ovine toxoplasmosis. Parasitology 136: 1887-1894.
30. Miller M, Conrad P, James ER, Packham A, Toy-Choutka S, et al. (2008) Transplacental toxoplasmosis in a wild southern sea otter (Enhydra lutris nereis). Vet Parasitol 153: 12-18.
31. Cornelissen AW, Overdulve JP (1985) Sex determination and sex differentiation in coccidia: gametogony and oocyst production after monoclonal infection of cats with free-living and intermediate host stages of Isospora (Toxoplasma) gondii. Parasitology 90(Pt 1): 35-44.
32. Pfefferkorn ER, Pfefferkorn LC, Colby ED (1977) Development of gametes and oocysts in cats fed cysts derived from cloned trophozoites of Toxoplasma gondii. J Parasitol 63: 158-159.
33. Miller MA, Conrad PA, Harris M, Hatfield B, Langlois G, et al. (2010) A protozoal-associated epizootic impacting marine wildlife: mass-mortality of southern sea otters (Enhydra lutris nereis) due to Sarcocystis neurona infection. Vet Parasitol 172: 183-194.
34. Wallace GD, Marshall L, Marshall M (1972) Cats, rats, and toxoplasmosis on a small Pacific island. Am J Epidemiol 95: 475-482.
35. Dubey JP, Rollor EA, Smith K, Kwok OC, Thulliez P (1997) Low seroprevalence of Toxoplasma gondii in feral pigs from a remote island lacking cats. J Parasitol 83: 839-841.
36. Munday BL (1972) Serological evidence of Toxoplasma infection in isolated groups of sheep. Res Vet Sci 13: 100-102.
37. Wallace GD (1969) Serologic and epidemiologic observations on toxoplasmosis on three Pacific atolls. Am J Epidemiol 90: 103-111.
38. de Moura L, Bahia-Oliveira LM, Wada MY, Jones JL, Tuboi SH, et al. (2006) Waterborne toxoplasmosis, Brazil, from field to gene. Emerg Infect Dis 12: 326-329.
39. Ajzenberg D, Dumetre A, Darde ML (2005) Multiplex PCR for typing strains of Toxoplasma gondii. J Clin Microbiol 43: 1940-1943.
40. Blackston CR, Dubey JP, Dotson E, Su C, Thulliez P, et al. (2001) Highresolution typing of Toxoplasma gondii using microsatellite loci. J Parasitol 87: 1472-1475.
41. Dubey JP, Navarro IT, Graham DH, Dahl E, Freire RL, et al. (2003) Characterization of Toxoplasma gondii isolates from free range chickens from Parana, Brazil. Vet Parasitol 117: 229-234.
42. Dubey JP, Navarro IT, Sreekumar C, Dahl E, Freire RL, et al. (2004) Toxoplasma gondii infections in cats from Parana, Brazil: seroprevalence, tissue distribution, and biologic and genetic characterization of isolates. J Parasitol 90: 721-726.
43. Dubey JP, Velmurugan GV, Chockalingam A, Pena HF, de Oliveira LN, et al. (2008) Genetic diversity of Toxoplasma gondii isolates from chickens from Brazil. Vet Parasitol 157: 299-305.
44. Vaudaux JD, Muccioli C, James ER, Silveira C, Magargal SL, et al. (2010) Identification of an atypical strain of Toxoplasma gondii as the cause of a waterborne outbreak of toxoplasmosis in Santa Isabel do Ivai, Brazil. J Infect Dis 202: 1226-1233.
45. Lehmann T, Graham DH, Dahl ER, Bahia-Oliveira LM, Gennari SM, et al. (2004) Variation in the structure of Toxoplasma gondii and the roles of selfing, drift, and epistatic selection in maintaining linkage disequilibria. Infect Genet Evol 4: 107-114.
46. Demar M, Ajzenberg D, Maubon D, Djossou F, Panchoe D, et al. (2007) Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clin Infect Dis 45: e88-e95.
47. Elsheikha HM, Schott HC, 2nd, Mansfield LS (2006) Genetic variation among isolates of Sarcocystis neurona, the agent of protozoal myeloencephalitis, as revealed by amplified fragment length polymorphism markers. Infect Immun 74: 3448-3454.
48. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) EBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186: 1518-1530.
49. Spratt BG, Hanage WP, Li B, Aanensen DM, Feil EJ (2004) Displaying the relatedness among isolates of bacterial species - the eBURST approach. FEMS Microbiol Lett 241: 129-134.
50. Turner KM, Hanage WP, Fraser C, Connor TR, Spratt BG (2007) Assessing the reliability of eBURST using simulated populations with known ancestry. BMC Microbiol 7: 30.
51. Smith JM, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci U S A 90: 4384-4388.
52. Arkush KD, Miller MA, Leutenegger CM, Gardner IA, Packham AE, et al. (2003) Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). Int J Parasitol 33: 1087-1097.
53. Lindsay DS, Collins MV, Mitchell SM, Wetch CN, Rosypal AC, et al. (2004) Survival of Toxoplasma gondii oocysts in Eastern oysters (Crassostrea virginica). J Parasitol 90: 1054-1057.
54. Miller MA, Miller WA, Conrad PA, James ER, Melli AC, et al. (2008) Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. Int J Parasitol 38: 1319-1328.
55. Ebert EE (1968) A Food Habits Study of Southern Sea Otter Enhydra Lutris Nereis. California Fish and Game 54: 33-37.
56. Thaipadungpanit J, Wuthiekanun V, Chierakul W, Smythe LD, Petkanchanapong W, et al. (2007) A dominant clone of Leptospira interrogans associated with an outbreak of human leptospirosis in Thailand. PLoS Negl Trop Dis 1: e56. doi:10.1371/journal.pntd.0000056.
57. Fisher MC, Koenig GL, White TJ, Taylor JW (2000) Pathogenic clones versus environmentally driven population increase: analysis of an epidemic of the human fungal pathogen Coccidioides immitis. J Clin Microbiol 38: 807-813.
58. Butcher M, Lakritz J, Halaney A, Branson K, Gupta GD, et al. (2002) Experimental inoculation of domestic cats (Felis domesticus) with Sarcocystis neurona or S. neurona-like merozoites. Vet Parasitol 107: 1-14.
59. Sibley LD (2003) Recent origins among ancient parasites. Vet Parasitol 115: 185-198.
60. Boughattas S, Ben-Abdallah R, Siala E, Souissi O, Aoun K, et al. (2010) Direct genotypic characterization of Toxoplasma gondii strains associated with congenital toxoplasmosis in Tunisia (North Africa). Am J Trop Med Hyg 82: 1041-1046.
61. Aspinall TV, Guy EC, Roberts KE, Joynson DH, Hyde JE, et al. (2003) Molecular evidence for multiple Toxoplasma gondii infections in individual patients in England and Wales: public health implications. Int J Parasitol 33: 97-103.
62. Dubey JP, Lopez-Torres HY, Sundar N, Velmurugan GV, Ajzenberg D, et al. (2007) Mouse-virulent Toxoplasma gondii isolated from feral cats on Mona Island, Puerto Rico. J Parasitol 93: 1365-1369.
63. Dubey JP, Moura L, Majumdar D, Sundar N, Velmurugan GV, et al. (2009) Isolation and characterization of viable Toxoplasma gondii isolates revealed possible high frequency of mixed infection in feral cats (Felis domesticus) from St Kitts, West Indies. Parasitology 136: 589-594.
64. Dubey JP, Su C, Cortes JA, Sundar N, Gomez-Marin JE, et al. (2006) Prevalence of Toxoplasma gondii in cats from Colombia, South America and genetic characterization of T. gondii isolates. Vet Parasitol 141: 42-47.
65. Dubey JP, Sundar N, Pineda N, Kyvsgaard NC, Luna LA, et al. (2006) Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Nicaragua, Central America. Vet Parasitol 142: 47-53.
66. Dubey JP, Vianna MC, Sousa S, Canada N, Meireles S, et al. (2006) Characterization of Toxoplasma gondii isolates in free-range chickens from Portugal. J Parasitol 92: 184-186.
67. Dubey JR, Bhaiyat MI, de Allie C, Macpherson CN, Sharma RN, et al. (2005) Isolation, tissue distribution, and molecular characterization of Toxoplasma gondii from chickens in Grenada, West Indies. J Parasitol 91: 557-560.
68. Elbez-Rubinstein A, Ajzenberg D, Darde ML, Cohen R, Dumetre A, et al. (2009) Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J Infect Dis 199: 280-285.
69. Lindstrom I, Sundar N, Lindh J, Kironde F, Kabasa JD, et al. (2008) Isolation and genotyping of Toxoplasma gondii from Ugandan chickens reveals frequent multiple infections. Parasitology 135: 39-45.
70. Ragozo AM, Pena HF, Yai LE, Su C, Gennari SM (2010) Genetic diversity among Toxoplasma gondii isolates of small ruminants from Brazil: novel genotypes revealed. Vet Parasitol 170: 307-312.
71. Sundar N, Cole RA, Thomas NJ, Majumdar D, Dubey JP, et al. (2008) Genetic diversity among sea otter isolates of Toxoplasma gondii. Vet Parasitol 151: 125-132.
72. Parameswaran N, Thompson RC, Sundar N, Pan S, Johnson M, et al. (2010) Non-archetypal Type II-like and atypical strains of Toxoplasma gondii infecting marsupials of Australia. Int J Parasitol 40: 635-640.
73. Fux B, Nawas J, Khan A, Gill DB, Su C, et al. (2007) Toxoplasma gondii strains defective in oral transmission are also defective in developmental stage differentiation. Infect Immun 75: 2580-2590.
74. Khan A, Fux B, Su C, Dubey JP, Darde ML, et al. (2007) Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Proc Natl Acad Sci U S A 104: 14872-14877.
75. Dubey JP (2001) Oocyst shedding by cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii to cats and mice. J Parasitol 87: 215-219.
76. Dubey JP (2006) Comparative infectivity of oocysts and bradyzoites of Toxoplasma gondii for intermediate (mice) and definitive (cats) hosts. Vet Parasitol 140: 69-75.
77. Dubey JP, Lunney JK, Shen SK, Kwok OC, Ashford DA, et al. (1996) Infectivity of low numbers of Toxoplasma gondii oocysts to pigs. J Parasitol 82: 438-443.
78. Mateus-Pinilla NE, Dubey JP, Choromanski L, Weigel RM (1999) A field trial of the effectiveness of a feline Toxoplasma gondii vaccine in reducing T. gondii exposure for swine. J Parasitol 85: 855-860.
79. Dubey JP, Lindsay DS, Saville WJ, Reed SM, Granstrom DE, et al. (2001) A review of Sarcocystis neurona and equine protozoal myeloencephalitis (EPM). Vet Parasitol 95: 89-131.
80. Mansfield LS, Mehler S, Nelsonc K, Elsheikha HM, Murphy AJ, et al. (2008) Brown-headed cowbirds (Molothrus ater) harbor Sarcocystis neurona and act as intermediate hosts. Vet Parasitol 153: 24-43.
81. Miller MA, Barr BC, Nordhausen R, James ER, Magargal SL, et al. (2009) Ultrastructural and molecular confirmation of the development of Sarcocystis neurona tissue cysts in the central nervous system of southern sea otters (Enhydra lutris nereis). Int J Parasitol 39: 1363-1372.
82. Costa KS, Santos SL, Uzeda RS, Pinheiro AM, Almeida MA, et al. (2008) Chickens (Gallus domesticus) are natural intermediate hosts of Neospora caninum. Int J Parasitol 38: 157-159.
83. Gondim LS, Abe-Sandes K, Uzeda RS, Silva MS, Santos SL, et al. (2010) Toxoplasma gondii and Neospora caninum in sparrows (Passer domesticus) in the Northeast of Brazil. Vet Parasitol 168: 121-124.
84. Heitman J (2010) Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8: 86-99.
85. Asmundsson IM, Rosenthal BM (2006) Isolation and characterization of microsatellite markers from Sarcocystis neurona, a causative agent of equine protozoal myeloencephalitis. Mol Ecol Notes 6: 8-10.