#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Self-Mating in the Definitive Host Potentiates Clonal Outbreaks of the Apicomplexan Parasites and


Tissue-encysting coccidia, including Toxoplasma gondii and Sarcocystis neurona, are heterogamous parasites with sexual and asexual life stages in definitive and intermediate hosts, respectively. During its sexual life stage, T. gondii reproduces either by genetic out-crossing or via clonal amplification of a single strain through self-mating. Out-crossing has been experimentally verified as a potent mechanism capable of producing offspring possessing a range of adaptive and virulence potentials. In contrast, selfing and other life history traits, such as asexual expansion of tissue-cysts by oral transmission among intermediate hosts, have been proposed to explain the genetic basis for the clonal population structure of T. gondii. In this study, we investigated the contributing roles self-mating and sexual recombination play in nature to maintain clonal population structures and produce or expand parasite clones capable of causing disease epidemics for two tissue encysting parasites. We applied high-resolution genotyping against strains isolated from a T. gondii waterborne outbreak that caused symptomatic disease in 155 immune-competent people in Brazil and a S. neurona outbreak that resulted in a mass mortality event in Southern sea otters. In both cases, a single, genetically distinct clone was found infecting outbreak-exposed individuals. Furthermore, the T. gondii outbreak clone was one of several apparently recombinant progeny recovered from the local environment. Since oocysts or sporocysts were the infectious form implicated in each outbreak, the expansion of the epidemic clone can be explained by self-mating. The results also show that out-crossing preceded selfing to produce the virulent T. gondii clone. For the tissue encysting coccidia, self-mating exists as a key adaptation potentiating the epidemic expansion and transmission of newly emerged parasite clones that can profoundly shape parasite population genetic structures or cause devastating disease outbreaks.


Vyšlo v časopise: Self-Mating in the Definitive Host Potentiates Clonal Outbreaks of the Apicomplexan Parasites and. PLoS Genet 6(12): e32767. doi:10.1371/journal.pgen.1001261
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001261

Souhrn

Tissue-encysting coccidia, including Toxoplasma gondii and Sarcocystis neurona, are heterogamous parasites with sexual and asexual life stages in definitive and intermediate hosts, respectively. During its sexual life stage, T. gondii reproduces either by genetic out-crossing or via clonal amplification of a single strain through self-mating. Out-crossing has been experimentally verified as a potent mechanism capable of producing offspring possessing a range of adaptive and virulence potentials. In contrast, selfing and other life history traits, such as asexual expansion of tissue-cysts by oral transmission among intermediate hosts, have been proposed to explain the genetic basis for the clonal population structure of T. gondii. In this study, we investigated the contributing roles self-mating and sexual recombination play in nature to maintain clonal population structures and produce or expand parasite clones capable of causing disease epidemics for two tissue encysting parasites. We applied high-resolution genotyping against strains isolated from a T. gondii waterborne outbreak that caused symptomatic disease in 155 immune-competent people in Brazil and a S. neurona outbreak that resulted in a mass mortality event in Southern sea otters. In both cases, a single, genetically distinct clone was found infecting outbreak-exposed individuals. Furthermore, the T. gondii outbreak clone was one of several apparently recombinant progeny recovered from the local environment. Since oocysts or sporocysts were the infectious form implicated in each outbreak, the expansion of the epidemic clone can be explained by self-mating. The results also show that out-crossing preceded selfing to produce the virulent T. gondii clone. For the tissue encysting coccidia, self-mating exists as a key adaptation potentiating the epidemic expansion and transmission of newly emerged parasite clones that can profoundly shape parasite population genetic structures or cause devastating disease outbreaks.


Zdroje

1. LiW

RaoultD

FournierPE

2009 Bacterial strain typing in the genomic era. FEMS Microbiol Rev 33 892 916

2. FeilEJ

SprattBG

2001 Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol 55 561 590

3. SmithGJ

VijaykrishnaD

BahlJ

LycettSJ

WorobeyM

2009 Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459 1122 1125

4. PowersC

DeFilippisV

MalouliD

FruhK

2008 Cytomegalovirus immune evasion. Curr Top Microbiol Immunol 325 333 359

5. Aires-de-SousaM

CorreiaB

de LencastreH

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. AmorimML

FariaNA

OliveiraDC

VasconcelosC

CabedaJC

2007 Changes in the clonal nature and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus isolates associated with spread of the EMRSA-15 clone in a tertiary care Portuguese hospital. J Clin Microbiol 45 2881 2888

7. FraserC

HanageWP

SprattBG

2005 Neutral microepidemic evolution of bacterial pathogens. Proc Natl Acad Sci U S A 102 1968 1973

8. OguraY

OokaT

IguchiA

TohH

AsadulghaniM

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. ReidSD

HerbelinCJ

BumbaughAC

SelanderRK

WhittamTS

2000 Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406 64 67

10. AkopyantsNS

KimblinN

SecundinoN

PatrickR

PetersN

2009 Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324 265 268

11. ByrnesEJIII

LiW

LewitY

MaH

VoelzK

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. FraserJA

GilesSS

WeninkEC

Geunes-BoyerSG

WrightJR

2005 Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437 1360 1364

13. BoyleJP

RajasekarB

SaeijJP

AjiokaJW

BerrimanM

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. GriggME

BonnefoyS

HehlAB

SuzukiY

BoothroydJC

2001 Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 294 161 165

15. GauntMW

YeoM

FrameIA

StothardJR

CarrascoHJ

2003 Mechanism of genetic exchange in American trypanosomes. Nature 421 936 939

16. JenniL

MartiS

SchweizerJ

BetschartB

Le PageRW

1986 Hybrid formation between African trypanosomes during cyclical transmission. Nature 322 173 175

17. AlyAS

VaughanAM

KappeSH

2009 Malaria parasite development in the mosquito and infection of the mammalian host. Annu Rev Microbiol 63 195 221

18. HoweDK

SibleyLD

1995 Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis 172 1561 1566

19. SuC

EvansD

ColeRH

KissingerJC

AjiokaJW

2003 Recent expansion of Toxoplasma through enhanced oral transmission. Science 299 414 416

20. GriggME

SundarN

2009 Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. Int J Parasitol 39 925 933

21. SibleyLD

AjiokaJW

2008 Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu Rev Microbiol 62 329 351

22. AsmundssonIM

DubeyJP

RosenthalBM

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. RejmanekD

MillerMA

GriggME

CrosbiePR

ConradPA

2010 Molecular characterization of Sarcocystis neurona strains from opossums (Didelphis virginiana) and intermediate hosts from Central California. Vet Parasitol 170 20 29

24. SundarN

AsmundssonIM

ThomasNJ

SamuelMD

DubeyJP

2008 Modest genetic differentiation among North American populations of Sarcocystis neurona may reflect expansion in its geographic range. Vet Parasitol 152 8 15

25. WendteJM

MillerMA

NandraAK

PeatSM

CrosbiePR

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. TibayrencM

AyalaFJ

2002 The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol 18 405 410

27. DubeyJP

2009 History of the discovery of the life cycle of Toxoplasma gondii. Int J Parasitol 39 877 882

28. HideG

MorleyEK

HughesJM

GerwashO

ElmahaishiMS

2009 Evidence for high levels of vertical transmission in Toxoplasma gondii. Parasitology 136 1877 1885

29. InnesEA

BartleyPM

BuxtonD

KatzerF

2009 Ovine toxoplasmosis. Parasitology 136 1887 1894

30. MillerM

ConradP

JamesER

PackhamA

Toy-ChoutkaS

2008 Transplacental toxoplasmosis in a wild southern sea otter (Enhydra lutris nereis). Vet Parasitol 153 12 18

31. CornelissenAW

OverdulveJP

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. PfefferkornER

PfefferkornLC

ColbyED

1977 Development of gametes and oocysts in cats fed cysts derived from cloned trophozoites of Toxoplasma gondii. J Parasitol 63 158 159

33. MillerMA

ConradPA

HarrisM

HatfieldB

LangloisG

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. WallaceGD

MarshallL

MarshallM

1972 Cats, rats, and toxoplasmosis on a small Pacific island. Am J Epidemiol 95 475 482

35. DubeyJP

RollorEA

SmithK

KwokOC

ThulliezP

1997 Low seroprevalence of Toxoplasma gondii in feral pigs from a remote island lacking cats. J Parasitol 83 839 841

36. MundayBL

1972 Serological evidence of Toxoplasma infection in isolated groups of sheep. Res Vet Sci 13 100 102

37. WallaceGD

1969 Serologic and epidemiologic observations on toxoplasmosis on three Pacific atolls. Am J Epidemiol 90 103 111

38. de MouraL

Bahia-OliveiraLM

WadaMY

JonesJL

TuboiSH

2006 Waterborne toxoplasmosis, Brazil, from field to gene. Emerg Infect Dis 12 326 329

39. AjzenbergD

DumetreA

DardeML

2005 Multiplex PCR for typing strains of Toxoplasma gondii. J Clin Microbiol 43 1940 1943

40. BlackstonCR

DubeyJP

DotsonE

SuC

ThulliezP

2001 High-resolution typing of Toxoplasma gondii using microsatellite loci. J Parasitol 87 1472 1475

41. DubeyJP

NavarroIT

GrahamDH

DahlE

FreireRL

2003 Characterization of Toxoplasma gondii isolates from free range chickens from Parana, Brazil. Vet Parasitol 117 229 234

42. DubeyJP

NavarroIT

SreekumarC

DahlE

FreireRL

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. DubeyJP

VelmuruganGV

ChockalingamA

PenaHF

de OliveiraLN

2008 Genetic diversity of Toxoplasma gondii isolates from chickens from Brazil. Vet Parasitol 157 299 305

44. VaudauxJD

MuccioliC

JamesER

SilveiraC

MagargalSL

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. LehmannT

GrahamDH

DahlER

Bahia-OliveiraLM

GennariSM

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. DemarM

AjzenbergD

MaubonD

DjossouF

PanchoeD

2007 Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clin Infect Dis 45 e88 95

47. ElsheikhaHM

SchottHC2nd

MansfieldLS

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. FeilEJ

LiBC

AanensenDM

HanageWP

SprattBG

2004 eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186 1518 1530

49. SprattBG

HanageWP

LiB

AanensenDM

FeilEJ

2004 Displaying the relatedness among isolates of bacterial species — the eBURST approach. FEMS Microbiol Lett 241 129 134

50. TurnerKM

HanageWP

FraserC

ConnorTR

SprattBG

2007 Assessing the reliability of eBURST using simulated populations with known ancestry. BMC Microbiol 7 30

51. SmithJM

SmithNH

O'RourkeM

SprattBG

1993 How clonal are bacteria? Proc Natl Acad Sci U S A 90 4384 4388

52. ArkushKD

MillerMA

LeuteneggerCM

GardnerIA

PackhamAE

2003 Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). Int J Parasitol 33 1087 1097

53. LindsayDS

CollinsMV

MitchellSM

WetchCN

RosypalAC

2004 Survival of Toxoplasma gondii oocysts in Eastern oysters (Crassostrea virginica). J Parasitol 90 1054 1057

54. MillerMA

MillerWA

ConradPA

JamesER

MelliAC

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. EbertEE

1968 A Food Habits Study of Southern Sea Otter Enhydra Lutris Nereis. California Fish and Game 54 33 37

56. ThaipadungpanitJ

WuthiekanunV

ChierakulW

SmytheLD

PetkanchanapongW

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. FisherMC

KoenigGL

WhiteTJ

TaylorJW

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. ButcherM

LakritzJ

HalaneyA

BransonK

GuptaGD

2002 Experimental inoculation of domestic cats (Felis domesticus) with Sarcocystis neurona or S. neurona-like merozoites. Vet Parasitol 107 1 14

59. SibleyLD

2003 Recent origins among ancient parasites. Vet Parasitol 115 185 198

60. BoughattasS

Ben-AbdallahR

SialaE

SouissiO

AounK

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. AspinallTV

GuyEC

RobertsKE

JoynsonDH

HydeJE

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. DubeyJP

Lopez-TorresHY

SundarN

VelmuruganGV

AjzenbergD

2007 Mouse-virulent Toxoplasma gondii isolated from feral cats on Mona Island, Puerto Rico. J Parasitol 93 1365 1369

63. DubeyJP

MouraL

MajumdarD

SundarN

VelmuruganGV

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. DubeyJP

SuC

CortesJA

SundarN

Gomez-MarinJE

2006 Prevalence of Toxoplasma gondii in cats from Colombia, South America and genetic characterization of T. gondii isolates. Vet Parasitol 141 42 47

65. DubeyJP

SundarN

PinedaN

KyvsgaardNC

LunaLA

2006 Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Nicaragua, Central America. Vet Parasitol 142 47 53

66. DubeyJP

ViannaMC

SousaS

CanadaN

MeirelesS

2006 Characterization of Toxoplasma gondii isolates in free-range chickens from Portugal. J Parasitol 92 184 186

67. DubeyJR

BhaiyatMI

de AllieC

MacphersonCN

SharmaRN

2005 Isolation, tissue distribution, and molecular characterization of Toxoplasma gondii from chickens in Grenada, West Indies. J Parasitol 91 557 560

68. Elbez-RubinsteinA

AjzenbergD

DardeML

CohenR

DumetreA

2009 Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J Infect Dis 199 280 285

69. LindstromI

SundarN

LindhJ

KirondeF

KabasaJD

2008 Isolation and genotyping of Toxoplasma gondii from Ugandan chickens reveals frequent multiple infections. Parasitology 135 39 45

70. RagozoAM

PenaHF

YaiLE

SuC

GennariSM

2010 Genetic diversity among Toxoplasma gondii isolates of small ruminants from Brazil: novel genotypes revealed. Vet Parasitol 170 307 312

71. SundarN

ColeRA

ThomasNJ

MajumdarD

DubeyJP

2008 Genetic diversity among sea otter isolates of Toxoplasma gondii. Vet Parasitol 151 125 132

72. ParameswaranN

ThompsonRC

SundarN

PanS

JohnsonM

2010 Non-archetypal Type II-like and atypical strains of Toxoplasma gondii infecting marsupials of Australia. Int J Parasitol 40 635 640

73. FuxB

NawasJ

KhanA

GillDB

SuC

2007 Toxoplasma gondii strains defective in oral transmission are also defective in developmental stage differentiation. Infect Immun 75 2580 2590

74. KhanA

FuxB

SuC

DubeyJP

DardeML

2007 Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Proc Natl Acad Sci U S A 104 14872 14877

75. DubeyJP

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. DubeyJP

2006 Comparative infectivity of oocysts and bradyzoites of Toxoplasma gondii for intermediate (mice) and definitive (cats) hosts. Vet Parasitol 140 69 75

77. DubeyJP

LunneyJK

ShenSK

KwokOC

AshfordDA

1996 Infectivity of low numbers of Toxoplasma gondii oocysts to pigs. J Parasitol 82 438 443

78. Mateus-PinillaNE

DubeyJP

ChoromanskiL

WeigelRM

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. DubeyJP

LindsayDS

SavilleWJ

ReedSM

GranstromDE

2001 A review of Sarcocystis neurona and equine protozoal myeloencephalitis (EPM). Vet Parasitol 95 89 131

80. MansfieldLS

MehlerS

NelsoncK

ElsheikhaHM

MurphyAJ

2008 Brown-headed cowbirds (Molothrus ater) harbor Sarcocystis neurona and act as intermediate hosts. Vet Parasitol 153 24 43

81. MillerMA

BarrBC

NordhausenR

JamesER

MagargalSL

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. CostaKS

SantosSL

UzedaRS

PinheiroAM

AlmeidaMA

2008 Chickens (Gallus domesticus) are natural intermediate hosts of Neospora caninum. Int J Parasitol 38 157 159

83. GondimLS

Abe-SandesK

UzedaRS

SilvaMS

SantosSL

2010 Toxoplasma gondii and Neospora caninum in sparrows (Passer domesticus) in the Northeast of Brazil. Vet Parasitol 168 121 124

84. HeitmanJ

2010 Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8 86 99

85. AsmundssonIM

RosenthalBM

2006 Isolation and characterization of microsatellite markers from Sarcocystis neurona, a causative agent of equine protozoal myeloencephalitis. Mol Ecol Notes 6 8 10

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2010 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#