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Low Diversity Variety Multilocus Sequence Types from Thailand Are Consistent with an Ancestral African Origin


The global burden of HIV-associated cryptococcal meningitis is estimated at nearly one million cases per year, causing up to a third of all AIDS-related deaths. Molecular epidemiology constitutes the main methodology for understanding the factors underpinning the emergence of this understudied, yet increasingly important, group of pathogenic fungi. Cryptococcus species are notable in the degree that virulence differs amongst lineages, and highly-virulent emerging lineages are changing patterns of human disease both temporally and spatially. Cryptococcus neoformans variety grubii (Cng, serotype A) constitutes the most ubiquitous cause of cryptococcal meningitis worldwide, however patterns of molecular diversity are understudied across some regions experiencing significant burdens of disease. We compared 183 clinical and environmental isolates of Cng from one such region, Thailand, Southeast Asia, against a global MLST database of 77 Cng isolates. Population genetic analyses showed that Thailand isolates from 11 provinces were highly homogenous, consisting of the same genetic background (globally known as VNI) and exhibiting only ten nearly identical sequence types (STs), with three (STs 44, 45 and 46) dominating our sample. This population contains significantly less diversity when compared against the global population of Cng, specifically Africa. Genetic diversity in Cng was significantly subdivided at the continental level with nearly half (47%) of the global STs unique to a genetically diverse and recombining population in Botswana. These patterns of diversity, when combined with evidence from haplotypic networks and coalescent analyses of global populations, are highly suggestive of an expansion of the Cng VNI clade out of Africa, leading to a limited number of genotypes founding the Asian populations. Divergence time testing estimates the time to the most common ancestor between the African and Asian populations to be 6,920 years ago (95% HPD 122.96 - 27,177.76). Further high-density sampling of global Cng STs is now necessary to resolve the temporal sequence underlying the global emergence of this human pathogen.


Vyšlo v časopise: Low Diversity Variety Multilocus Sequence Types from Thailand Are Consistent with an Ancestral African Origin. PLoS Pathog 7(4): e32767. doi:10.1371/journal.ppat.1001343
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001343

Souhrn

The global burden of HIV-associated cryptococcal meningitis is estimated at nearly one million cases per year, causing up to a third of all AIDS-related deaths. Molecular epidemiology constitutes the main methodology for understanding the factors underpinning the emergence of this understudied, yet increasingly important, group of pathogenic fungi. Cryptococcus species are notable in the degree that virulence differs amongst lineages, and highly-virulent emerging lineages are changing patterns of human disease both temporally and spatially. Cryptococcus neoformans variety grubii (Cng, serotype A) constitutes the most ubiquitous cause of cryptococcal meningitis worldwide, however patterns of molecular diversity are understudied across some regions experiencing significant burdens of disease. We compared 183 clinical and environmental isolates of Cng from one such region, Thailand, Southeast Asia, against a global MLST database of 77 Cng isolates. Population genetic analyses showed that Thailand isolates from 11 provinces were highly homogenous, consisting of the same genetic background (globally known as VNI) and exhibiting only ten nearly identical sequence types (STs), with three (STs 44, 45 and 46) dominating our sample. This population contains significantly less diversity when compared against the global population of Cng, specifically Africa. Genetic diversity in Cng was significantly subdivided at the continental level with nearly half (47%) of the global STs unique to a genetically diverse and recombining population in Botswana. These patterns of diversity, when combined with evidence from haplotypic networks and coalescent analyses of global populations, are highly suggestive of an expansion of the Cng VNI clade out of Africa, leading to a limited number of genotypes founding the Asian populations. Divergence time testing estimates the time to the most common ancestor between the African and Asian populations to be 6,920 years ago (95% HPD 122.96 - 27,177.76). Further high-density sampling of global Cng STs is now necessary to resolve the temporal sequence underlying the global emergence of this human pathogen.


Zdroje

1. MitchellTG

PerfectJR

1995 Cryptococcosis in the era of AIDS—100 years after the discovery of Cryptococcus neoformans. Clin Microbiol Rev 8 515 548

2. KingJ

DasguptaA

2005 Cryptococcosis. Updated 30th October, 2009. Available: http://emedicine.medscape.com/article/215354-overview. Accessed 24 April 2010.

3. 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

4. BanerjeeU

DattaK

MajumdarT

GuptaK

2001 Cryptococcosis in India: the awakening of a giant? Med Mycol 39 51 67

5. StevensDA

DenningDW

ShatskyS

ArmstrongRW

AdlerJD

1999 Cryptococcal meningitis in the immunocompromised host: intracranial hypertension and other complications. Mycopathologia 146 1 8

6. DayJ

2004 Cryptococcal meningitis. Pract Neurol 4 274 285

7. SchutteCM

Van der MeydenCH

MagaziDS

2000 The impact of HIV on meningitis as seen at a South African Academic Hospital (1994 to 1998). Infection 28 3 7

8. BicanicT

HarrisonTS

2004 Cryptococcal meningitis. Br Med Bull 72 99 118

9. FranzotSP

SalkinIF

CasadevallA

1999 Cryptococcus neoformans var. grubii: Separate varietal status for Cryptococcus neoformans serotype A isolates. J Clin Microbiol 37 838 840

10. Kwon-ChungKJ

BoekhoutT

FellJW

DiazM

2002 (1557) Proposal to conserve the name Cryptococcus gattii against C. hondurianus and C. bacillisporus (Basidiomycota, Hymenomycetes, Tremellomycetidae). Taxon 51 804 806

11. BoversM

HagenF

KuramaeE

DiazM

SpanjaardL

2006 Unique hybrids between the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. FEMS Yeast Res 6 599 607

12. BoversM

HagenF

BoekhoutT

2008 Diversity of the Cryptococcus neoformans (Cryptococcus gattii) species. Rev Iberoam Micol 25 S4 12

13. 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

14. BoekhoutT

TheelenB

DiazM

FellJW

HopWCJ

2001 Hybrid genotypes in the pathogenic yeast Cryptococcus neoformans. Microbiology 147 891 907

15. MeyerW

CastanedaA

JacksonS

HuynhM

CastanedaE

2003 Molecular typing of IberoAmerican Cryptococcus neoformans isolates. Emerg Infect Dis 9 189 195

16. SukroongreungS

NilakulC

RuangsomboonO

ChuakulW

EampokalapB

1996 Serotypes of Cryptococcus neoformans isolated from patients prior to and during the AIDS era in Thailand. Mycopathologia 135 75 78

17. TayST

LimHC

TajuddinTH

RohaniMY

HamimahH

2006 Determination of molecular types and genetic heterogeneity of Cryptococcus neoformans and C. gattii in Malaysia. Med Mycol 44 617 622

18. Kwon-ChungKJ

BennettJE

1978 Distribution of alpha and a mating types of Cryptococcus neoformans among natural and clinical Isolates. Am J Epidemiol 108 337 340

19. YanZ

LiXG

XuJP

2002 Geographic distribution of mating type alleles of Cryptococcusneoformans in four areas of the United States. J Clin Microbiol 40 965 972

20. HallidayCL

BuiT

KrockenbergerM

MalikR

EllisDH

1999 Presence of alpha and a mating types in environmental and clinical collections of Cryptococcus neoformans var. gattii strains from Australia. J Clin Microbiol 37 2920 2926

21. MadrenysN

DevroeyC

RaeswuytackC

TorresrodriguezJM

1993 Identification of the perfect state of Cryptococcus neoformans from 195 clinical isolates including 84 from AIDS patients.. Mycopathologia 123 65 68

22. Barreto de OliveiraMT

BoekhoutT

TheelenB

HagenF

BaroniFA

2004 Cryptococcus neoformans shows a remarkable genotypic diversity in Brazil. J Clin Microbiol 42 1356 1359

23. OhkusuM

TangonanN

TakeoK

KishidaE

OhkuboM

2002 Serotype, mating type and ploidy of Cryptococcus neoformans strains isolated from patients in Brazil. Rev Inst Med Trop S Paulo 44 299 302

24. Kwon-ChungKJ

1974 Genetics of fungi pathogenic for man. CRC Cr Rev Microbiol 3 115 133

25. PadhyeAA

CarmichaelJW

1969 Mating behavior of Trichophyton mentagrphytes varieties paried with Arthroderma benhamiae mating types. Sabouraudia 7 178 181

26. PadhyeAA

AjelloL

1977 Taxonomic status of hedgehog fungus Trichophyton erinacei. Sabouraudia 15 103 114

27. Kwon-ChungKJ

1975 Perfect state (Emmonsiella capsulata) of fungus causing large form African histoplasmosis. Mycologia 67 980 990

28. Kwon-ChungKJ

WeeksRJ

LarshHW

1974 Studies on Emmonsiella capsulata (Histoplasma capsulatum): II. Distribution of two mating types in 13 endemic states of the United States. Am J Epidemiol 99 44 49

29. RandhawaHS

KowshikT

KhanZU

2003 Decayed wood of Syzygium cumini and Ficus religiosa living trees in Delhi/New Delhi metropolitan area as natural habitat of Cryptococcus neoformans. Med Mycol 41 199 209

30. NishikawaMM

LazeraMS

BarbosaGG

TrillesL

BalassianoBR

2003 Serotyping of 467 Cryptococcus neoformans isolates from clinical and environmental sources in Brazil: analysis of host and regional patterns. J Clin Microbiol 41 73 77

31. CasadevallA

PerfectJR

1998 Cryptococcus neoformans. Washington D.C. ASM Press

32. VivianiMA

EspostoMC

CogliatiM

MontagnaMT

WickesBL

2001 Isolation of a Cryptococcus neoformans serotype A MATa strain from the Italian environment. Med Mycol 39 383 386

33. Kwon-Chung KJBJ

1992 Mucormycosis. Medical Mycology Philadelphia Lea & Febiger

34. JainN

WickesBL

KellerSA

FuJ

CasadevallA

2005 Molecular epidemiology of clinical Cryptococcus neoformans strains from India. J Clin Microbiol 43 5733 5742

35. ChenJ

VarmaA

DiazM

LitvintsevaA

WollenbergK

2008 Cryptococcus neoformans strains and infection in apparently immunocompetent patients, China. Emerg Infect Dis 14 755 762

36. ChenS

SorrellT

NimmoG

SpeedB

CurrieB

2000 Epidemiology and host- and variety-dependent characteristics of infection due to Cryptococcus neoformans in Australia and New Zealand. Clin Infect Dis 31 499 508

37. LitvintsevaAP

ThakurR

VilgalysR

MitchellTG

2006 Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. grubii (Serotype A), including a unique population in Botswana. Genetics 172 2223 2238

38. PitisuttithumP

TansuphasawadikulS

SimpsonAJH

HowePA

WhiteNJ

2001 A prospective study of AIDS-associated cryptococcal meningitis in Thailand treated with high-dose amphotericin B. J Infection 43 226 233

39. Illnait-ZaragoziMT

Martinez-MachinGF

Fernandez-AndreuCM

BoekhoutT

MeisJF

2010 Microsatellite typing of clinical and environmental Cryptococcus neoformans var. grubii isolates from Cuba shows multiple genetic lineages. Plos One 5 2 e9124 doi:10.1371/journal.pone.0009124.t004

40. 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 USA 101 17258 17263

41. LitvintsevaAP

KestenbaumL

VilgalysR

MitchellTG

2005 Comparative analysis of environmental and clinical populations of Cryptococcus neoformans. J Clin Microbiol 43 556 564

42. ByrnesEJ

LiW

LewitY

MaH

VoelzK

2010 Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog 6 4 e1000850 doi:10.1371/journal.ppat.1000850

43. MeyerW

MarszewskaK

AmirmostofianM

IgrejaRP

HardtkeC

1999 Molecular typing of global isolates of Cryptococcus neoformans var. neoformans by polymerase chain reaction fingerprinting and randomly amplified polymorphic DNA - a pilot study to standardize techniques on which to base a detailed epidemiological survey. Electrophoresis 20 1790 1799

44. MeyerW

AanensenDM

BoekhoutT

CogliatiM

DiazMR

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

45. WolfeN

DunavanC

DiamondJ

2007 Origins of major human infectious diseases. Nature 447 279 283

46. FalushD

WirthT

LinzB

PritchardJ

StephensM

2003 Traces of human migrations in Helicobacter pylori populations. Science 299 1582 1585

47. FisherM

KoenigG

WhiteT

San-BlasG

NegroniR

2001 Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration. Proc Natl Acad Sci 98 4558 4562

48. FraserJA

GilesSS

WeninkEC

Geunes-BoyerSG

WrightJR

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

49. JohnstonR

1992 Birds of North America. Philadelphia American Ornithologist's Union and Academy of Natural Sciences Of Philadelphia

50. LinX

HeitmanJ

2006 The biology of the Cryptococcus neoformans species complex. Annu Rev Microbiol 60 69 105

51. Swinne-DesgainD

1976 Cryptococcus neoformans in Crops of Pigeons Following Its Experimental Administration. Sabouraudia 14 313 317

52. MooneyHAHRJ

2000 Invasive species in a changing world. Washington DC Island Press Washington DC

53. GrzimekBSN

OlendorfD

2004 Grzimek's animal life encyclopedia. Farmington Hills, Michigan Gale

54. PappagianisD

EinsteinH

1978 Tempest from Tehachapi takes toll or Coccidioides conveyed aloft and afar. West J Med 129 527 530

55. ArchibaldLK

McDonaldLC

RheanpumikankitS

TansuphaswadikulS

ChaovanichA

1999 Fever and Human Immunodeficiency Virus infection as sentinels for emerging mycobacterial and fungal bloodstream infections in hospitalized patients >/ = 15 years old, Bangkok. J Infect Dis 180 87 92

56. LitvintsevaAP

MarraRE

NielsenK

HeitmanJ

VilgalysR

2003 Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot Cell 2 1162 1168

57. NgamskulrungrojP

GilgadoF

FaganelloJ

LitvintsevaAP

LealAL

2009 Genetic diversity of the Cryptococcus species complex suggests that Cryptococcus gattii deserves to have varieties. PLoS ONE 4 6 e5862 doi:10.1371/journal.pone.0005862

58. BurtA

CarterDA

KoenigGL

WhiteTJ

TaylorJW

1996 Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. Proc Natl Acad Sci 93 770 773

59. AgapowPM

BurtA

2001 Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1 101 102

60. BennettRS

MilgroomMG

BergstromGC

2005 Population structure of seedborne Phaeosphaeria nodorum on New York wheat. Phytopathology 95 300 305

61. HudsonRR

KaplanNL

1985 Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111 147 164

62. TajimaF

1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 585 595

63. Ramos-OnsinsSE

RozasJ

2006 Statistical properties of new neutrality tests against population growth (vol 19, pg 2092, 2002). Mol Biol Evol 23 1642 1642

64. NeiM

1987 Molecular Evolutionary Genetics. New York Columbia University Press

65. HudsonRR

BoosDD

KaplanNL

1992 A Statistical test for detecting geographic subdivision. Mol Biol Evol 9 138 151

66. HudsonRR

2000 A new statistic for detecting genetic differentiation. Genetics 155 2011 2014

67. KasugaT

WhiteTJ

TaylorJW

2002 Estimation of nucleotide substitution rates in eurotiomycete fungi. Mol Biol Evol 19 2318 2324

68. BrouwerAE

RajanuwongA

ChierakulW

GriffinGE

LarsenRA

2004 Combination antifungal therapies for HIV-associated cryptococcal meningitis: a randomised trial. Lancet 363 1764 1767

69. WrightP

InverarityD

2007 Human immunodeficiency virus (HIV) related cryptococcal meningitis in rural central Thailand - treatment difficulties and prevention strategies. Southeast Asian J Trop Med Public Health 38 58 61

70. McClellandCM

ChangYC

VarmaA

Kwon-ChungKJ

2004 Uniqueness of the mating system in Cryptococcus neoformans. Trends Microbiol 12 208 212

71. Kwon-ChungKJ

BennettJE

1978 Distribution of alpha and alpha mating types of Cryptococcus neoformans among natural and clinical isolates. Am J Epidemiol 108 337 340

72. CasaliAK

GoulartL

SilvaLKR

SilvaKRE

RibeiroAM

2003 Molecular typing of clinical and environmental Cryptococcus neoformans isolates in the Brazilian state Rio Grande do Sul. FEMS Yeast Res 3 405 415

73. HiremathSS

ChowdharyA

KowshikT

RandhawaHS

SunS

2008 Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiology 154 1513 1524

74. TaylorJW

GeiserDM

BurtA

KoufopanouV

1999 The evolutionary biology and population genetics underlying fungal strain typing. Clin Microbiol Rev 12 126 146

75. BuchananKL

MurphyJW

1998 What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 4 71 83

76. LinXR

HullCM

HeitmanJ

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

77. BuiT

LinX

MalikR

HeitmanJ

CarterD

2008 Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, alpha mating type populations. Eukaryot Cell 7 1771 1780

78. XuJP

MitchellTG

2003 Comparative gene genealogical analyses of strains of serotype AD identify recombination in populations of serotypes A and D in the human pathogenic yeast Cryptococcus neoformans. Microbiology 149 2147 2154

79. LinXR

PatelS

LitvintsevaAP

FloydA

MitchellTG

2009 Diploids in the Cryptococcus neoformans serotype A population homozygous for the alpha mating type originate via unisexual mating. Plos Pathogens 5 1 e1000283 doi:10.1371/journal.ppat.1000283

80. SribureeP

KhayhanS

KhamwanC

PanjaiseeS

TharavichitkulP

2004 Serotype and PCR-fingerprints of clinical and environmental isolates of Cryptococcus neoformans in Chiang Mai, Thailand. Mycopathologia 158 25 31

81. LengelerKB

CoxGM

HeitmanJ

2001 Serotype AD strains of Cryptococcus neoformans are diploid or aneuploid and are heterozygous at the mating-type locus. Infect Immun 69 115 122

82. TamuraK

DudleyJ

NeiM

KumarS

2007 MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

83. PeakallR

SmousePE

2006 GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6 288 295

84. ExcoffierL

SmousePE

QuattroJM

1992 Analysis of molecular variance inferred from metric distances among DNA haplotypes - application to human mitochondrial-DNA restriction data. Genetics 131 479 491

85. JombartT

2008 adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24 1403 1405

86. DoledecS

ChesselD

1987 Seasonal successions and spatial variables in fresh-water environments. 1. Description of a complete 2-way layout by projection of variables. Acta Oecol-Oec Gen 8 403 426

87. SaitouN

NeiM

1987 The Neighbor-joining method - a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406 425

88. FelsensteinJ

1985 Confidence-limits on phylogenies - an approach using the bootstrap. Evolution 39 783 791

89. PerfectJR

KetabchiN

CoxGM

IngramCW

BeiserCL

1993 Karyotyping of Cryptococcus neoformans as an epidemiological tool. J Clin Microbiol 31 3305 3309

90. BrownAHD

FeldmanMW

NevoE

1980 Multilocus structure of natural populations of Hordeum spontaneum. Genetics 96 523 536

91. SmithJM

SmithNH

OrourkeM

SprattBG

1993 How clonal are bacteria. Proc Natl Acad Sci 90 4384 4388

92. EstabrookGF

LandrumL

1975 A simple test for the possible simultaneous evolutionary divergence of two amino acid positions. Taxon 24 609 613

93. XuJP

YanZ

GuoH

2009 Divergence, hybridization, and recombination in the mitochondrial genome of the human pathogenic yeast Cryptococcus gattii. Mol Ecol 18 2628 2642

94. LibradoP

RozasJ

2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 1451 1452

95. WattersonGA

1975 Number of segregating sites in genetic models without recombination. Theor Popul Biol 7 256 276

96. Drummond AJHS

RawlenceN

RambautA

2007 A rough guide to BEAST 1.4. Available: http://beast.bio.ed.ac.uk/Main_Page. Accessed 11 November 2009

97. ClementM

PosadaD

CrandallKA

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

98. 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

99. Ramos-OnsinsSE

RozasJ

2002 Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19 2092 2100

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