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Clonality Despite Sex: The Evolution of Host-Associated Sexual Neighborhoods in the Pathogenic Fungus


Molecular genetic approaches typically detect recombination in microbes regardless of assumed asexuality. However, genetic data have shown the AIDS-associated pathogen Penicillium marneffei to have extensive spatial genetic structure at local and regional scales, and although there has been some genetic evidence that a sexual cycle is possible, this haploid fungus is thought to be genetically, as well as morphologically, asexual in nature because of its highly clonal population structure. Here we use comparative genomics, experimental mixed-genotype infections, and population genetic data to elucidate the role of recombination in natural populations of P. marneffei. Genome wide comparisons reveal that all the genes required for meiosis are present in P. marneffei, mating type genes are arranged in a similar manner to that found in other heterothallic fungi, and there is evidence of a putatively meiosis-specific mutational process. Experiments suggest that recombination between isolates of compatible mating types may occur during mammal infection. Population genetic data from 34 isolates from bamboo rats in India, Thailand and Vietnam, and 273 isolates from humans in China, India, Thailand, and Vietnam show that recombination is most likely to occur across spatially and genetically limited distances in natural populations resulting in highly clonal population structure yet sexually reproducing populations. Predicted distributions of three different spatial genetic clusters within P. marneffei overlap with three different bamboo rat host distributions suggesting that recombination within hosts may act to maintain population barriers within P. marneffei.


Vyšlo v časopise: Clonality Despite Sex: The Evolution of Host-Associated Sexual Neighborhoods in the Pathogenic Fungus. PLoS Pathog 8(10): e32767. doi:10.1371/journal.ppat.1002851
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002851

Souhrn

Molecular genetic approaches typically detect recombination in microbes regardless of assumed asexuality. However, genetic data have shown the AIDS-associated pathogen Penicillium marneffei to have extensive spatial genetic structure at local and regional scales, and although there has been some genetic evidence that a sexual cycle is possible, this haploid fungus is thought to be genetically, as well as morphologically, asexual in nature because of its highly clonal population structure. Here we use comparative genomics, experimental mixed-genotype infections, and population genetic data to elucidate the role of recombination in natural populations of P. marneffei. Genome wide comparisons reveal that all the genes required for meiosis are present in P. marneffei, mating type genes are arranged in a similar manner to that found in other heterothallic fungi, and there is evidence of a putatively meiosis-specific mutational process. Experiments suggest that recombination between isolates of compatible mating types may occur during mammal infection. Population genetic data from 34 isolates from bamboo rats in India, Thailand and Vietnam, and 273 isolates from humans in China, India, Thailand, and Vietnam show that recombination is most likely to occur across spatially and genetically limited distances in natural populations resulting in highly clonal population structure yet sexually reproducing populations. Predicted distributions of three different spatial genetic clusters within P. marneffei overlap with three different bamboo rat host distributions suggesting that recombination within hosts may act to maintain population barriers within P. marneffei.


Zdroje

1. de WitR, BouvierT (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8: 755–758.

2. FinlayBJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063.

3. GreenJL, BohannanBJM, WhitakerRJ (2008) Microbial biogeography: From taxonomy to traits. Science 320: 1039–1043.

4. RydholmC, SzakacsG, LutzoniF (2006) Low genetic variation and no detectable population structure in Aspergillus fumigatus compared to closely related Neosartorya species. Eukaryot Cell 5: 650–657.

5. HenkDA, EagleCE, BrownK, Van Den BergMA, DyerPS, et al. (2011) Speciation despite globally overlapping distributions in Penicillium chrysogenum: the population genetics of Alexander Fleming's lucky fungus. Mol Ecol 4288–4301.

6. HeitmanJ (2006) Sexual reproduction and the evolution of microbial pathogens. Curr Biol 16: R711–R725.

7. HeitmanJ (2010) Evolution of eukaryotic microbial pathogens via covert sexual Reproduction. Cell Host Microbe 8: 86–99.

8. SunS, HeitmanJ (2011) Is sex necessary? BMC Biol 9: 56.

9. BarrettLG, ThrallPH, BurdonJJ, LindeCC (2008) Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol 23: 678–685.

10. BruyndonckxN, HenryI, ChristeP, KerthG (2009) Spatio-temporal population genetic structure of the parasitic mite Spinturnix bechsteini is shaped by its own demography and the social system of its bat host. Mol Ecol 18: 3581–3592.

11. FisherMC, AanensenD, de HoogS, VanittanakomN (2004) Multilocus microsatellite typing system for Penicillium marneffei reveals spatially structured populations. J Clin Microbol 42: 5065–5069.

12. KasugaT, WhiteTJ, KoenigG, McewenJ, RestrepoA, et al. (2003) Phylogeography of the fungal pathogen Histoplasma capsulatum. Mol Ecol 12: 3383–3401.

13. MeeceJK, AndersonJL, FisherMC, HenkDA, SlossBL, et al. (2011) Population genetic structure of clinical and environmental isolates of Blastomyces dermatitidis, based on 27 polymorphic microsatellite markers. App Environ Microb 77: 5123–5131.

14. NeafseyDE, BarkerBM, SharptonTJ, StajichJE, ParkDJ, et al. (2010) Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res 20: 938–946.

15. SimwamiSP, KhayhanK, HenkDA, AanensenDM, BoekhoutT, et al. (2011) Low diversity Cryptococcus neoformans Variety grubii multilocus sequence types from Thailand are consistent with an ancestral african origin. PLoS Pathog 7: e1001343.

16. LeeSC, NiM, LiWJ, ShertzC, HeitmanJ (2010) The Evolution of Sex: a perspective from the fungal kingdom. Microbiol Mol Biol R 74: 298–340.

17. BilliardS, Lopez-VillavicencioM, DevierB, HoodME, FairheadC, et al. (2011) Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol Rev 86: 421–442.

18. FisherMC, KoenigGL, WhiteTJ, San-BlasG, NegroniR, et al. (2001) Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration. Proc Natl Acad Sci USA 98: 4558–4562.

19. LitvintsevaAP, LinX, TempletonI, HeitmanJ, MitchellTG (2007) Many globally isolated AD hybrid strains of Cryptococcus neoformans originated in Africa. PLoS Pathog 3: 1109–1117.

20. KasugaT, TaylorJW, WhiteTJ (1999) Phylogenetic relationships of varieties and geographical groups of the human pathogenic fungus Histoplasma capsulatum Darling. J Clin Microbiol 37: 653–663.

21. TaylorML, Chavez-TapiaCB, Rojas-MartinezA, Reyes-MontesMD, del ValleMB, et al. (2005) Geographical distribution of genetic polymorphism of the pathogen Histoplasma capsulatum isolated from infected bats, captured in a central zone of Mexico. FEMS Immunol Med Mic 45: 451–458.

22. LinXR, HullCM, HeitmanJ (2005) Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434: 1017–1021.

23. LitvintsevaAP, MarraRE, NielsenK, HeitmanJ, VilgalysR, et al. (2003) Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot Cell 2: 1162–1168.

24. FisherMC, HanageWP, de HoogS, JohnsonE, SmithMD, et al. (2005) Low effective dispersal of asexual genotypes in heterogeneous landscapes by the endemic pathogen Penicillium marneffei. PLoS Pathog 1: 159–165.

25. WooPCY, ChongKTK, TseH, CaiJJ, LauCCY, et al. (2006) Genomic and experimental evidence for a potential sexual cycle in the pathogenic thermal dimorphic fungus Penicillium marneffei. FEBS Lett 580: 4976–4977.

26. SegretainG (1959) Penicillium marneffei n.sp., agent of a mycosis of the reticuloendothelial system. Mycopathologia 11: 327–353.

27. FisherMC, de HoogGS, VannittanakomN (2004) A highly discriminatory Multilocus Microsatellite Typing System (MLMT) for Penicillium marneffei. Mol Ecol Notes 5: 231–234.

28. PeakallR, SmousePE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288–295.

29. JombartT (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.

30. WarrenDL, GlorRE, TurelliM (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62: 2868–2883.

31. LebloisR, EstoupA, RoussetF (2009) IBDSim: a computer program to simulate genotypic data under isolation by distance. Mol Ecol Resour 9: 107–109.

32. ForcheA, AlbyK, SchaeferD, JohnsonAD, BermanJ, et al. (2008) The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 6: 1084–1097.

33. GalaganJE, SelkerEU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20: 417–423.

34. KeeneyS, GirouxCN, KlecknerN (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375–384.

35. PoggelerS (2002) Genomic evidence for mating abilities in the asexual pathogen Aspergillus fumigatus. Curr Genet 42: 153–160.

36. TzungKW, WilliamsRM, SchererS, FederspielN, JonesT, et al. (2001) Genomic evidence for a complete sexual cycle in Candida albicans. Proc Natl Acad Sci USA 98: 3249–3253.

37. Dyer PS (2007) Sexual reproduction and significance of MAT in the Aspergilli. In: Sex in fungi: molecular determination and evolutionary implications. Heitman J, Kronstad, J.W, Taylor, J.W, and Casselton, L.A., editors. Washington, DC: ASM Press. pp. 123–142.

38. SelkerEU (1990) Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 24: 579–613.

39. ClutterbuckAJ (2011) Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 48: 306–326.

40. BraumannI, van den BergM, KempkenF (2008) Repeat induced point mutation in two asexual fungi, Aspergillus niger and Penicillium chrysogenum. Curr Genet 53: 287–297.

41. FreitagM, WilliamsRL, KotheGO, SelkerEU (2002) A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Natl Acad Sci USA 99: 8802–8807.

42. MalagnacF, WendelB, GoyonC, FaugeronG, ZicklerD, et al. (1997) A gene essential for de novo methylation and development in ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell 91: 281–290.

43. O'GormanCM, FullerHT, DyerPS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457: 471–U475.

44. NeuvegliseC, SarfatiJ, LatgeJP, ParisS (1996) Afut1, a retrotransposon-like element from Aspergillus fumigatus. Nucleic Acids Res 24: 1428–1434.

45. WrightS (1965) The interpretation of population structure by F-Statistics with special regard to systems of mating. Evolution 19: 395–420.

46. JombartT, DevillardS, DufourAB, PontierD (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101: 92–103.

47. JombartT, DrayS, DufourAB (2009) Finding essential scales of spatial variation in ecological data: a multivariate approach. Ecography 32: 161–168.

48. DettmanJR, TaylorJW (2004) Mutation and evolution of microsatellite loci in neurospora. Genetics 168: 1231–1248.

49. RuderferDM, PrattSC, SeidelHS, KruglyakL (2006) Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 38: 1077–1081.

50. HudsonRR, KaplanNL (1985) Statistical Properties of the Number of Recombination Events in the History of a Sample of DNA-Sequences. Genetics 111: 147–164.

51. WrightS (1931) Evolution in Mendelian Populations. Genetics 16: 97–159.

52. LeslieJF, KleinKK (1996) Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics 144: 557–567.

53. 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.

54. 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.

55. FraserJA, GilesSS, WeninkEC, Geunes-BoyerSG, WrightJR, et al. (2005) Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437: 1360–1364.

56. 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.

57. KaweckiTJ, EbertD (2004) Conceptual issues in local adaptation. Ecol Lett 7: 1225–1241.

58. RundleHD, NosilP (2005) Ecological speciation. Ecol Lett 8: 336–352.

59. SchluterD, ConteGL (2009) Genetics and ecological speciation. Proc Natl Acad Sci USA 106: 9955–9962.

60. EganSP, NosilP, FunkDJ (2008) Selection and genomic differentiation during ecological speciation: Isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62: 1162–1181.

61. HendryAP, NosilP, RiesebergLH (2007) The speed of ecological speciation. Funct Ecol 21: 455–464.

62. ViaS (2002) The ecological genetics of speciation. Am Nat 159: S1–S7.

63. GiraudT, RefregierG, Le GacM, de VienneDM, HoodME (2008) Speciation in fungi. Fungal Genet Biol 45: 791–802.

64. PhillipsSJ, AndersonRP, SchapireRE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190: 231–259.

65. LiangL, CaoCW, WangWJ, LuoH, HuangSB, et al. (2011) Common Reservoirs for Penicillium marneffei Infection in Humans and Rodents, China. Emerg Infect Dis 17: 209–214.

66. WarrenDL, GlorRE, TurelliM (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33: 607–611.

67. GladieuxP, VerckenE, FontaineMC, HoodME, JonotO, et al. (2011) Maintenance of fungal pathogen species that are specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol 28: 459–471.

68. HullCM, RaisnerRM, JohnsonAD (2000) Evidence for mating of the “asexual” yeast Candida albicans in a mammalian host. Science 289: 307–310.

69. HsuehYP, HeitmanJ (2008) Orchestration of sexual reproduction and virulence by the fungal mating-type locus. Curr Opin Microbiol 11: 517–524.

70. GiraudT, YocktengR, Lopez-VillavicencioM, RefregierG, HoodME (2008) Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryot Cell 7: 765–775.

71. KohnLM (2005) Mechanisms of fungal speciation. Annu Rev Phytopathol 43: 279–308.

72. Fisher MC (2007) The evolutionary implications of an asexual lifestyle manifested by Penicillium marneffei. In: Sex in fungi: molecular determination and evolutionary implications. Heitman J, Kronstad JW, Taylor JW, Casselton LA, editors. Washington, DC: ASM Press. pp. 201–212.

73. CharlesworthD, WillisJH (2009) The genetics of inbreeding depression. Nat Rev Genet 10: 783–796.

74. Goddard MR (2007) Why bother with sex? Answers from experiments with yeast and other organisms. In: Sex in fungi: molecular determination and evolutionary implications. Heitman J, Kronstad, J.W, Taylor, J.W, and Casselton, L.A., editors. Washington, DC: ASM Press. pp. 489–506.

75. BruggemanJ, DebetsAJM, WijngaardenPJ, deVisserJAGM, HoekstraRF (2003) Sex slows down the accumulation of deleterious mutations in the homothallic fungus Aspergillus nidulans. Genetics 164: 479–485.

76. Lopez-VillavicencioM, AguiletaG, GiraudT, de VienneDM, LacosteS, et al. (2010) Sex in Penicillium: Combined phylogenetic and experimental approaches. Fungal Genet Biol 47: 693–706.

77. GeiserDM (2009) Sexual structures in Aspergillus: morphology, importance and genomics. Med Mycolo 47 Suppl 1: S21–26.

78. NelsonMA, MetzenbergRL (1992) Sexual development genes of Neurospora Crassa. Genetics 132: 149–162.

79. BahnYS, XueCY, IdnurmA, RutherfordJC, HeitmanJ, et al. (2007) Sensing the environment: lessons from fungi. Nature Reviews Microbiology 5: 57–69.

80. WangP, PerfectJR, HeitmanJ (2000) The G-protein beta subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. J Mol Cell Biol 20: 352–362.

81. GrishkanI, KorolAB, NevoE, WasserSP (2003) Ecological stress and sex evolution in soil microfungi. Proc Biol Sci 270: 13–18.

82. Alonso-MongeR, RomanE, AranaDM, PlaJ, NombelaC (2009) Fungi sensing environmental stress. Clin Microbiol Infec 15: 17–19.

83. Kwon-ChungKJ (1972) Emmonsiella capsulata: perfect state of Histoplasma capsulatum. Science 177: 368–369.

84. McDonoughES, LewisAL (1967) Blastomyces dermatitidis: production of the sexual stage. Science 156: 528–529.

85. RougeronV, De MeeusT, HideM, WaleckxE, BermudezH, et al. (2009) Extreme inbreeding in Leishmania braziliensis. Proc Natl Acad Sci USA 106: 10224–10229.

86. RougeronV, BanulsAL, CarmeB, SimonS, CouppieP, et al. (2011) Reproductive strategies and population structure in Leishmania: substantial amount of sex in Leishmania viannia guyanensis. Mol Ecol 20: 3116–3127.

87. DyeC, WilliamsBG (1997) Multigenic drug resistance among inbred malaria parasites. Proc R Soc Lond B Biol Sci 264: 61–67.

88. RazakandrainibeFG, DurandP, KoellaJC, De MeeusT, RoussetF, et al. (2005) “Clonal” population structure of the malaria agent Plasmodium falciparum in high-infection regions. Proc Natl Acad Sci USA 102: 17388–17393.

89. DubeyJP, VelmuruganGV, RajendranC, YabsleyMJ, ThomasNJ, et al. (2011) Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type. International J Parasitol 41: 1139–1147.

90. WendteJM, MillerMA, LambournDM, MagargalSL, JessupDA, et al. (2010) Self-mating in the definitive host potentiates clonal outbreaks of the apicomplexan parasites Sarcocystis neurona and Toxoplasma gondii. PLoS Genet 6: e1001261.

91. AlbyK, SchaeferD, BennettRJ (2009) Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460: 890–893.

92. NielsenK, De ObaldiaAL, HeitmanJ (2007) Cryptococcus neoformans mates on pigeon guano: Implications for the realized ecological niche and globalization. Eukaryot Cell 6: 949–959.

93. XueCY, TadaY, DoingXN, HeitmanJ (2007) The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1: 263–273.

94. BuiT, LinXR, 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.

95. LinXR (2009) Cryptococcus neoformans: Morphogenesis, infection, and evolution. Infect Genet Evol 9: 401–416.

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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