Emergence and Pathogenicity of Highly Virulent Genotypes in the Northwest United States

English version České info

Cryptococcus gattii causes life-threatening disease in otherwise healthy hosts and to a lesser extent in immunocompromised hosts. The highest incidence for this disease is on Vancouver Island, Canada, where an outbreak is expanding into neighboring regions including mainland British Columbia and the United States. This outbreak is caused predominantly by C. gattii molecular type VGII, specifically VGIIa/major. In addition, a novel genotype, VGIIc, has emerged in Oregon and is now a major source of illness in the region. Through molecular epidemiology and population analysis of MLST and VNTR markers, we show that the VGIIc group is clonal and hypothesize it arose recently. The VGIIa/IIc outbreak lineages are sexually fertile and studies support ongoing recombination in the global VGII population. This illustrates two hallmarks of emerging outbreaks: high clonality and the emergence of novel genotypes via recombination. In macrophage and murine infections, the novel VGIIc genotype and VGIIa/major isolates from the United States are highly virulent compared to similar non-outbreak VGIIa/major-related isolates. Combined MLST-VNTR analysis distinguishes clonal expansion of the VGIIa/major outbreak genotype from related but distinguishable less-virulent genotypes isolated from other geographic regions. Our evidence documents emerging hypervirulent genotypes in the United States that may expand further and provides insight into the possible molecular and geographic origins of the outbreak.

Vyšlo v časopise: Emergence and Pathogenicity of Highly Virulent Genotypes in the Northwest United States. PLoS Pathog 6(4): e32767. doi:10.1371/journal.ppat.1000850
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000850

Souhrn

Zdroje

1. MorensDM

FolkersGK

FauciAS

2004 The challenge of emerging and re-emerging infectious diseases. Nature 430 242 249

2. CohenML

2000 Changing patterns of infectious disease. Nature 406 762 767

3. JonesKE

PatelNG

LevyMA

StoreygardA

BalkD

2008 Global trends in emerging infectious diseases. Nature 451 990 993

4. PappasC

AguilarPV

BaslerCF

SolorzanoA

ZengH

2008 Single gene reassortants identify a critical role for PB1, HA, and NA in the high virulence of the 1918 pandemic influenza virus. Proc Natl Acad Sci U S A 105 3064 3069

5. HeitmanJ

2006 Sexual reproduction and the evolution of microbial pathogens. Curr Biol 16 R711 725

6. FraserJA

GilesSS

WeninkEC

Geunes-BoyerSG

WrightJR

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

7. 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

8. GriggME

SuzukiY

2003 Sexual recombination and clonal evolution of virulence in Toxoplasma. Microbes Infect 5 685 690

9. ReidSD

HerbelinCJ

BumbaughAC

SelanderRK

WhittamTS

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

10. CasadevallA

PirofskiL

2001 Host-pathogen interactions: the attributes of virulence. J Infect Dis 184 337 344

11. LiW

RaoultD

FournierPE

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

12. KiddSE

HagenF

TscharkeRL

HuynhM

BartlettKH

2004 A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci U S A 101 17258 17263

13. ByrnesEJ3rd

BildfellRJ

FrankSA

MitchellTG

MarrKA

2009 Molecular evidence that the range of the Vancouver Island outbreak of Cryptococcus gattii infection has expanded into the Pacific Northwest in the United States. J Infect Dis 199 1081 1086

14. ByrnesEJ3rd

BildfellRJ

DearingPL

ValentineBA

HeitmanJ

2009 Cryptococcus gattii with bimorphic colony types in a dog in western Oregon: additional evidence for expansion of the Vancouver Island outbreak. J Vet Diagn Invest 21 133 136

15. MacDougallL

KiddSE

GalanisE

MakS

LeslieMJ

2007 Spread of Cryptococcus gattii in British Columbia, Canada, and detection in the Pacific Northwest, USA. Emerg Infect Dis 13 42 50

16. BartlettKH

KiddSE

KronstadJW

2008 The emergence of Cryptococcus gattii in British Columbia and the Pacific Northwest. Curr Infect Dis Rep 10 58 65

17. DattaK

BartlettKH

BaerR

ByrnesE

GalanisE

2009 Spread of Cryptococcus gattii into Pacific Northwest region of the United States. Emerg Infect Dis 15 1185 1191

18. UptonA

FraserJA

KiddSE

BretzC

BartlettKH

2007 First contemporary case of human infection with Cryptococcus gattii in Puget Sound: evidence for spread of the Vancouver Island outbreak. J Clin Microbiol 45 3086 3088

19. Kwon-ChungKJ

BennettJE

1984 Epidemiologic differences between the two varieties of Cryptococcus neoformans. Am J Epidemiol 120 123 130

20. Kwon-ChungKJ

BennettJE

1984 High prevalence of Cryptococcus neoformans var. gattii in tropical and subtropical regions. Zentralbl Bakteriol Mikrobiol Hyg [A] 257 213 218

21. SorrellTC

2001 Cryptococcus neoformans variety gattii. Med Mycol 39 155 168

22. Kwon-ChungKJ

BoekhoutT

FellJW

DiazM

2002 Proposal to conserve the name Cryptococcus gattii against C. hondurianus and C. bacillisporus (Basidiomycota, Hymenomycetes, Tremellomycetidae) Taxon 51 804 806

23. CasadevallA

PerfectJ

1998 Cryptococcus neoformans Washington DC ASM Press

24. ParkBJ

WannemuehlerKA

MarstonBJ

GovenderN

PappasPG

2009 Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. Aids 23 525 530

25. PerfectJR

1989 Cryptococcosis. Infect Dis Clin North Am 3 77 102

26. KiddSE

ChowY

MakS

BachPJ

ChenH

2007 Characterization of environmental sources of the human and animal pathogen Cryptococcus gattii in British Columbia, Canada, and the Pacific Northwest of the United States. Appl Environ Microbiol 73 1433 1443

27. MacDougallL

FyfeM

2006 Emergence of Cryptococcus gattii in a novel environment provides clues to its incubation period. J Clin Microbiol 44 1851 1852

28. MeyerW

AanensenDM

BoekhoutT

CogliatiM

DiazMR

2009 Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococcus gattii. Med Mycol 47 561 570

29. BoversM

HagenF

KuramaeEE

BoekhoutT

2008 Six monophyletic lineages identified within Cryptococcus neoformans and Cryptococcus gattii by multi-locus sequence typing. Fungal Genet Biol 45 400 421

30. JamesTY

LitvintsevaAP

VilgalysR

MorganJA

TaylorJW

2009 Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog 5 e1000458 doi:10.1371/journal.ppat.1000458

31. MaH

HagenF

StekelDJ

JohnstonSA

SionovE

2009 The fatal fungal outbreak on Vancouver Island is characterized by enhanced intracellular parasitism driven by mitochondrial regulation. Proc Natl Acad Sci U S A 106 12980 12985

32. MaidenMC

BygravesJA

FeilE

MorelliG

RussellJE

1998 Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95 3140 3145

33. CarterDA

TaylorJW

DechairoB

BurtA

KoenigGL

2001 Amplified single-nucleotide polymorphisms and a (GA)(n) microsatellite marker reveal genetic differentiation between populations of Histoplasma capsulatum from the Americas. Fungal Genet Biol 34 37 48

34. 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

35. BensonG

1999 Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27 573 580

36. FraserJA

SubaranRL

NicholsCB

HeitmanJ

2003 Recapitulation of the sexual cycle of the primary fungal pathogen Cryptococcus neoformans var. gattii: implications for an outbreak on Vancouver Island, Canada. Eukaryot Cell 2 1036 1045

37. AltschulSF

MaddenTL

SchafferAA

ZhangJ

ZhangZ

1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402

38. ThompsonJD

HigginsDG

GibsonTJ

1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673 4680

39. KumarS

TamuraK

NeiM

2004 MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5 150 163

40. DereeperA

GuignonV

BlancG

AudicS

BuffetS

2008 Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36 W465 469

41. GuindonS

GascuelO

2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 696 704

42. ClementM

PosadaD

CrandallKA

2000 TCS: a computer program to estimate gene genealogies. Mol Ecol 9 1657 1659

43. MaH

CroudaceJE

LammasDA

MayRC

2006 Expulsion of live pathogenic yeast by macrophages. Curr Biol 16 2156 2160

44. VelagapudiR

HsuehYP

Geunes-BoyerS

WrightJR

HeitmanJ

2009 Spores as infectious propagules of Cryptococcus neoformans. Infect Immun 77 4345 4355

45. ChaturvediS

RenP

NarasipuraSD

ChaturvediV

2005 Selection of optimal host strain for molecular pathogenesis studies on Cryptococcus gattii. Mycopathologia 160 207 215

46. KiddSE

GuoH

BartlettKH

XuJ

KronstadJW

2005 Comparative gene genealogies indicate that two clonal lineages of Cryptococcus gattii in British Columbia resemble strains from other geographical areas. Eukaryot Cell 4 1629 1638

47. ByrnesEJ3rd

HeitmanJ

2009 Cryptococcus gattii outbreak expands into the Northwestern United States with fatal consequences. F1000 Biology Reports 1 62

48. PfeifferT

EllisD

1991 Environmental isolation of Cryptococcus neoformans var. gattii from California. J Infect Dis 163 929 930

49. CarterD

SaulN

CampbellLT

TienB

KrockenbergerM

2007 Sex in natural populations of C. gattii. Sex in Fungi: Molecular determination and evolutionary implications.

HeitmanJ

KronstadJW

TaylorJ

CasseltonL

ASM Press 477 488

50. SaulN

KrockenbergerM

CarterD

2008 Evidence of recombination in mixed-mating-type and alpha-only populations of Cryptococcus gattii sourced from single eucalyptus tree hollows. Eukaryot Cell 7 727 734

51. PerfectJR

LangSD

DurackDT

1980 Chronic cryptococcal meningitis: a new experimental model in rabbits. Am J Pathol 101 177 194

52. StephenC

LesterS

BlackW

FyfeM

RavertyS

2002 Multispecies outbreak of cryptococcosis on southern Vancouver Island, British Columbia. Can Vet J 43 792 794

53. DuncanC

SchwantjeH

StephenC

CampbellJ

BartlettK

2006 Cryptococcus gattii in wildlife of Vancouver Island, British Columbia, Canada. J Wildl Dis 42 175 178

54. CampbellLT

CurrieBJ

KrockenbergerM

MalikR

MeyerW

2005 Clonality and recombination in genetically differentiated subgroups of Cryptococcus gattii. Eukaryot Cell 4 1403 1409

55. CarterD

CampbellLT

SaulN

KrockenbergerM

2010 Sexual reproduction of Cryptococcus gattii: a papulation genetics perspective.

HeitmanJ

T.K

Kwon-ChungJ

PerfectJR

CasadevallA

Cryptococcus: ASM Press

56. XueC

TadaY

DongX

HeitmanJ

2007 The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1 263 273

57. Kwon-ChungKJ

1976 Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68 821 833

58. Kwon-ChungKJ

1976 A new species of Filobasidiella, the sexual state of Cryptococcus neoformans B and C serotypes. Mycologia 68 943 946

59. LinX

HullCM

HeitmanJ

2005 Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434 1017 1021

60. SukroongreungS

KitiniyomK

NilakulC

TantimavanichS

1998 Pathogenicity of basidiospores of Filobasidiella neoformans var. neoformans. Med Mycol 36 419 424

61. ZimmerBL

HempelHO

GoodmanNL

1984 Pathogenicity of the basidiospores of Filobasidiella neoformans. Mycopathologia 85 149 153

62. GilesSS

DagenaisTR

BottsMR

KellerNP

HullCM

2009 Elucidating the pathogenesis of spores from the human fungal pathogen Cryptococcus neoformans. Infect Immun 77 3491 3500

63. KiddSE

BachPJ

HingstonAO

MakS

ChowY

2007 Cryptococcus gattii dispersal mechanisms, British Columbia, Canada. Emerg Infect Dis 13 51 57

64. BoversM

HagenF

KuramaeEE

BoekhoutT

2009 Promiscuous mitochondria in Cryptococcus gattii. FEMS Yeast Res 9 489 503

65. XuJ

YanZ

GuoH

2009 Divergence, hybridization, and recombination in the mitochondrial genome of the human pathogenic yeast Cryptococcus gattii. Mol Ecol 12 2628 42

66. CampbellLT

CarterDA

2006 Looking for sex in the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. FEMS Yeast Res 6 588 598

67. CampbellLT

FraserJA

NicholsCB

DietrichFS

CarterD

2005 Clinical and environmental isolates of Cryptococcus gattii from Australia that retain sexual fecundity. Eukaryot Cell 4 1410 1419

68. NielsenK

De ObaldiaAL

HeitmanJ

2007 Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot Cell 6 949 959

69. HagenF

AssenSV

LuijckxGJ

BoekhoutT

KampingaGA

2009 Activated dormant Cryptococcus gattii infection in a Dutch tourist who visited Vancouver Island (Canada): a molecular epidemiological approach. Med Mycol Epub

70. LindbergJ

HagenF

LaursenA

StenderupJ

BoekhoutT

2007 Cryptococcus gattii risk for tourists visiting Vancouver Island, Canada. Emerg Infect Dis 13 178 179

71. BlankenshipJR

SinghN

AlexanderBD

HeitmanJ

2005 Cryptococcus neoformans isolates from transplant recipients are not selected for resistance to calcineurin inhibitors by current immunosuppressive regimens. J Clin Microbiol 43 464 467

72. ByrnesEJIII

LiW

LewitY

PerfectJR

CarterDA

2009 First reported case of Cryptococcus gattii in the Southeastern USA: implications for travel-associated acquisition of an emerging pathogen. PLoS ONE 4 e5851 doi:10.1371/journal.pone.0005851

73. MillerWG

PadhyeAA

van BonnW

JensenE

BrandtME

2002 Cryptococcosis in a bottlenose dolphin (Tursiops truncatus) caused by Cryptococcus neoformans var. gattii. J Clin Microbiol 40 721 724

74. ChaturvediS

DyavaiahM

LarsenRA

ChaturvediV

2005 Cryptococcus gattii in AIDS patients, southern California. Emerg Infect Dis 11 1686 1692

75. OlivaresLR