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PMID: 9880478 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S. Review

The evolutionary biology and population genetics underlying fungal strain typing.

Clinical microbiology reviews ·Vol. 12 ·No. 1 ·1999-01-00 ·Pages 126-46

Taylor JW, Geiser DM, Burt A, Koufopanou V

Abstract

Strain typing of medically important fungi and fungal population genetics have been stimulated by new methods of tapping DNA variation. The aim of this contribution is to show how awareness of fungal population genetics can increase the utility of strain typing to better serve the interests of medical mycology. Knowing two basic features of fungal population biology, the mode of reproduction and genetic differentiation or isolation, can give medical mycologists information about the intraspecific groups that are worth identifying and the number and type of markers that would be needed to do so. The same evolutionary information can be just as valuable for the selection of fungi for development and testing of pharmaceuticals or vaccines. The many methods of analyzing DNA variation are evaluated in light of the need for polymorphic loci that are well characterized, simple, independent, and stable. Traditional population genetic and new phylogenetic methods for analyzing mode of reproduction, genetic differentiation, and isolation are reviewed. Strain typing and population genetic reports are examined for six medically important species: Coccidioides immitis, Histoplasma capsulatum, Candida albicans, Cryptococcus neoformans, Aspergillus fumigatus, and A. flavus. Research opportunities in the areas of genomics, correlation of clinical variation with genetic variation, amount of recombination, and standardization of approach are suggested.

MeSH Terms
Biological Evolution Fungi/classification,genetics Genetics, Population Mycological Typing Techniques
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Taylor J W
Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102, USA. [email protected]
Geiser D M
Burt A
Koufopanou V
References (93)
93 references, click to expand
  1. Evolutionary relationships within the fungi: analyses of nuclear small subunit rRNA sequences.
    Mol Phylogenet Evol. 1992 Sep;1(3):231-41 PMID: 1342940
  2. Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs.
    Science. 1992 Apr 3;256(5053):100-2 PMID: 1348870
  3. Typing of Histoplasma capsulatum by restriction fragment length polymorphisms in a nuclear gene.
    J Clin Microbiol. 1992 Aug;30(8):2104-7 PMID: 1354224
  4. Electrophoretic karyotypes of clinical isolates of Coccidioides immitis.
    Infect Immun. 1992 Nov;60(11):4872-80 PMID: 1398998
  5. Recombination and the multilocus structure of fungal populations.
    Annu Rev Phytopathol. 1996;34:457-77 PMID: 15012552
  6. Are eukaryotic microorganisms clonal or sexual? A population genetics vantage.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5129-33 PMID: 1675793
  7. Isolation by Distance.
    Genetics. 1943 Mar;28(2):114-38 PMID: 17247074
  8. Multilocus Structure of Natural Populations of HORDEUM SPONTANEUM.
    Genetics. 1980 Oct;96(2):523-36 PMID: 17249067
  9. Classification of fungal chitin synthases.
    Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):519-23 PMID: 1731323
  10. A fungal gene for antibiotic resistance on a dispensable ("B") chromosome.
    Science. 1991 Dec 20;254(5039):1773-6 PMID: 1763326
  11. Clonality in soilborne, plant-pathogenic fungi.
    Annu Rev Phytopathol. 1995;33:369-91 PMID: 18999966
  12. Recombination in Escherichia coli and the definition of biological species.
    J Bacteriol. 1991 Nov;173(22):7257-68 PMID: 1938920
  13. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers.
    Nucleic Acids Res. 1990 Nov 25;18(22):6531-5 PMID: 1979162
  14. Telomeric and dispersed repeat sequences in Candida yeasts and their use in strain identification.
    J Bacteriol. 1991 Jan;173(2):842-50 PMID: 1987167
  15. Evolutionary relationships among pathogenic Candida species and relatives.
    J Bacteriol. 1991 Apr;173(7):2250-5 PMID: 2007550
  16. Combining data in phylogenetic analysis.
    Trends Ecol Evol. 1996 Apr;11(4):152-8 PMID: 21237790
  17. Natural habitat of Cryptococcus neoformans var. gattii.
    J Clin Microbiol. 1990 Jul;28(7):1642-4 PMID: 2199524
  18. Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2766-70 PMID: 2565038
  19. Use of mitochondrial and ribosomal DNA polymorphisms to classify clinical and soil isolates of Histoplasma capsulatum.
    Infect Immun. 1989 May;57(5):1409-12 PMID: 2565290
  20. Electrophoretic analysis of Histoplasma capsulatum chromosomal DNA.
    Mol Cell Biol. 1989 Mar;9(3):983-7 PMID: 2725508
  21. STRAINS OF NEUROSPORA COLLECTED FROM NATURE.
    Evolution. 1976 Jun;30(2):281-313 PMID: 28563048
  22. ESTIMATION OF GENE FLOW FROM F-STATISTICS.
    Evolution. 1993 Jun;47(3):855-863 PMID: 28567899
  23. Phylogenetic analysis of polymorphic DNA sequences at the Adh locus in Drosophila melanogaster and its sibling species.
    J Mol Evol. 1985;22(4):289-300 PMID: 3003368
  24. Classification of Histoplasma capsulatum isolates by restriction fragment polymorphisms.
    J Bacteriol. 1986 Mar;165(3):813-8 PMID: 3005239
  25. A Candida albicans dispersed, repeated gene family and its epidemiologic applications.
    Proc Natl Acad Sci U S A. 1988 Mar;85(5):1452-6 PMID: 3278313
  26. Epidemiology of coccidioidomycosis.
    Curr Top Med Mycol. 1988;2:199-238 PMID: 3288356
  27. Variation of electrophoretic karyotypes among clinical isolates of Candida albicans.
    J Clin Microbiol. 1988 May;26(5):842-5 PMID: 3290238
  28. Electrophoretic karyotypes and chromosome numbers in Candida species.
    J Gen Microbiol. 1987 Feb;133(2):425-30 PMID: 3309156
  29. Sexual stage of Histoplasma capsulatum.
    Science. 1972 Jan 21;175(4019):326 PMID: 4651892
  30. Taxonomic studies on Filobasidiella species and their anamorphs.
    Antonie Van Leeuwenhoek. 1982;48(1):25-38 PMID: 7046630
  31. Mating types and convertibility among soil isolates of Histoplasma capsulatum.
    Mycologia. 1980 Mar-Apr;72(2):404-6 PMID: 7383051
  32. AFLP: a new technique for DNA fingerprinting.
    Nucleic Acids Res. 1995 Nov 11;23(21):4407-14 PMID: 7501463
  33. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals.
    Microbiology. 1995 Jul;141 ( Pt 7):1507-21 PMID: 7551019
  34. Comparison of four DNA-based methods for strain delineation of Candida lusitaniae.
    J Clin Microbiol. 1995 Jun;33(6):1467-70 PMID: 7650168
  35. Colonizing populations of Candida albicans are clonal in origin but undergo microevolution through C1 fragment reorganization as demonstrated by DNA fingerprinting and C1 sequencing.
    J Clin Microbiol. 1995 Jun;33(6):1501-9 PMID: 7650175
  36. Comparison of three typing methods for clinical and environmental isolates of Aspergillus fumigatus.
    J Clin Microbiol. 1995 Jun;33(6):1596-601 PMID: 7650194
  37. A new genus, filobasidiella, the perfect state of Cryptococcus neoformans.
    Mycologia. 1975 Nov-Dec;67(6):1197-200 PMID: 765816
  38. Comparison of multilocus enzyme electrophoresis and random amplified polymorphic DNA analysis for molecular subtyping of Cryptococcus neoformans. The Cryplococcal Disease Active Surveillance Group.
    J Clin Microbiol. 1995 Jul;33(7):1890-5 PMID: 7665665
  39. Genetic population structure and gene flow in the Atlantic cod Gadus morhua: a comparison of allozyme and nuclear RFLP loci.
    Genetics. 1995 Jan;139(1):375-85 PMID: 7705638
  40. Malassezia and Trichosporon: two emerging pathogenic basidiomycetous yeast-like fungi.
    J Med Vet Mycol. 1994;32 Suppl 1:367-78 PMID: 7722799
  41. Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny.
    Science. 1995 Jun 9;268(5216):1492-5 PMID: 7770775
  42. Phylogeny of dermatophytes and dimorphic fungi based on large subunit ribosomal RNA sequence comparisons.
    J Med Vet Mycol. 1994;32(5):331-41 PMID: 7844699
  43. Characterization of Coccidioides immitis isolates by restriction fragment length polymorphisms.
    J Clin Microbiol. 1994 Dec;32(12):3040-2 PMID: 7883896
  44. Sexual origins of British Aspergillus nidulans isolates.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2349-52 PMID: 7907796
  45. Evidence for a phylogenetic connection between Coccidioides immitis and Uncinocarpus reesii (Onygenaceae).
    Microbiology. 1994 Jun;140 ( Pt 6):1481-94 PMID: 7915941
  46. DNA sequencing with arbitrary primer pairs.
    Mol Ecol. 1994 Oct;3(5):523-5 PMID: 7952333
  47. Comparison of the electrophoretic karyotypes and chromosomal location of ten genes in the two varieties of Cryptococcus neoformans.
    Microbiology. 1994 Mar;140 ( Pt 3):543-50 PMID: 8012577
  48. Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina.
    Genetics. 1994 Apr;136(4):1307-17 PMID: 8013907
  49. How can the low levels of DNA sequence variation in regions of the drosophila genome with low recombination rates be explained?
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6815-8 PMID: 8041702
  50. Oligonucleotide fingerprinting of isolates of Candida species other than C. albicans and of atypical Candida species from human immunodeficiency virus-positive and AIDS patients.
    J Clin Microbiol. 1993 Aug;31(8):2124-33 PMID: 8103773
  51. Use of DNA moderately repetitive sequence to type Aspergillus fumigatus isolates from aspergilloma patients.
    J Infect Dis. 1994 Mar;169(3):683-5 PMID: 8158052
  52. Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences.
    Proc Natl Acad Sci U S A. 1994 May 10;91(10):4599-603 PMID: 8183955
  53. Molecular epidemiology of nosocomial invasive aspergillosis.
    J Clin Microbiol. 1994 Mar;32(3):684-90 PMID: 8195379
  54. Multilocus enzyme typing of Cryptococcus neoformans.
    J Clin Microbiol. 1993 Oct;31(10):2819-23 PMID: 8253996
  55. The yeast Candida albicans has a clonal mode of reproduction in a population of infected human immunodeficiency virus-positive patients.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9456-9 PMID: 8415722
  56. Application of polymerase chain reaction to fingerprinting Aspergillus fumigatus by random amplification of polymorphic DNA.
    J Clin Microbiol. 1993 May;31(5):1117-21 PMID: 8501211
  57. How clonal are bacteria?
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4384-8 PMID: 8506277
  58. Chromosome-length polymorphism in fungi.
    Microbiol Rev. 1995 Dec;59(4):686-98 PMID: 8531892
  59. Phenotypic and genotypic analysis of variability in Aspergillus fumigatus.
    J Clin Microbiol. 1995 Oct;33(10):2567-75 PMID: 8567884
  60. Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis.
    Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):770-3 PMID: 8570632
  61. Genetic relatedness of Cryptococcus neoformans clinical isolates grouped with the repetitive DNA probe CNRE-1.
    J Clin Microbiol. 1995 Nov;33(11):2818-22 PMID: 8576325
  62. Wild chromosomal variants in Aspergillus nidulans.
    Curr Genet. 1996 Feb;29(3):293-300 PMID: 8595677
  63. Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the alpha-mating type.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7327-31 PMID: 8692992
  64. Typing Candida albicans oral isolates from human immunodeficiency virus-infected patients by multilocus enzyme electrophoresis and DNA fingerprinting.
    J Clin Microbiol. 1996 May;34(5):1235-48 PMID: 8727910
  65. Karyotype instability in Cryptococcus neoformans infection.
    J Clin Microbiol. 1996 Jun;34(6):1531-4 PMID: 8735111
  66. Loss of meiosis in Aspergillus.
    Mol Biol Evol. 1996 Jul;13(6):809-17 PMID: 8754217
  67. Molecular epidemiology of apparent outbreak of invasive aspergillosis in a hematology ward.
    J Clin Microbiol. 1996 Feb;34(2):345-51 PMID: 8789013
  68. Human pathogeneic fungi and their close nonpathogenic relatives.
    Mol Phylogenet Evol. 1996 Aug;6(1):89-96 PMID: 8812309
  69. Molecular subtype distribution of Cryptococcus neoformans in four areas of the United States. Cryptococcal Disease Active Surveillance Group.
    J Clin Microbiol. 1996 Apr;34(4):912-7 PMID: 8815107
  70. Relationships among pathogenic and nonpathogenic isolates of Fusarium oxysporum based on the partial sequence of the intergenic spacer region of the ribosomal DNA.
    Mol Plant Microbe Interact. 1996 Mar;9(2):125-38 PMID: 8820752
  71. Use of polymorphic short and clustered coding-region microsatellites to distinguish strains of Candida albicans.
    FEMS Immunol Med Microbiol. 1996 Sep;15(2-3):73-9 PMID: 8880131
  72. Multicentric epidemiological study of Aspergillus fumigatus isolates by multilocus enzyme electrophoresis.
    J Clin Microbiol. 1996 Oct;34(10):2559-68 PMID: 8880520
  73. Clinical isolates of Histoplasma capsulatum from Indianapolis, Indiana, have a recombining population structure.
    J Clin Microbiol. 1996 Oct;34(10):2577-84 PMID: 8880523
  74. Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12473-7 PMID: 8901606
  75. Molecular typing of Aspergillus fumigatus strains by sequence-specific DNA primer (SSDP) analysis.
    FEMS Immunol Med Microbiol. 1997 Feb;17(2):95-102 PMID: 9061355
  76. Molecular typing of Cryptococcus neoformans: taxonomic and epidemiological aspects.
    Int J Syst Bacteriol. 1997 Apr;47(2):432-42 PMID: 9103633
  77. Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5' end of the large-subunit (26S) ribosomal DNA gene.
    J Clin Microbiol. 1997 May;35(5):1216-23 PMID: 9114410
  78. Concordance of gene genealogies reveals reproductive isolation in the pathogenic fungus Coccidioides immitis.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5478-82 PMID: 9144263
  79. Amplified fragment length polymorphism (AFLP) fingerprinting of symbiotic fungi cultured by the fungus-growing ant Cyphomyrmex minutus.
    Mol Ecol. 1996 Feb;5(1):119-22 PMID: 9147688
  80. Comparison of four molecular typing methods for evaluating genetic diversity among Candida albicans isolates from human immunodeficiency virus-positive patients with oral candidiasis.
    J Clin Microbiol. 1997 Apr;35(4):856-61 PMID: 9157142
  81. Comparative analysis of genetic variability among Candida albicans isolates from different geographic locales by three genotypic methods.
    J Clin Microbiol. 1997 Jun;35(6):1332-6 PMID: 9163439
  82. Microsatellite polymorphism in the promoter sequence of the elongation factor 3 gene of Candida albicans as the basis for a typing system.
    J Clin Microbiol. 1997 Jul;35(7):1777-80 PMID: 9196192
  83. DNA variation at the Sod locus of Drosophila melanogaster: an unfolding story of natural selection.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7725-9 PMID: 9223255
  84. Are Candida albicans natural populations subdivided?
    Trends Microbiol. 1997 Jul;5(7):253-4; discussion 254-7 PMID: 9234499
  85. Genetic diversity among clinical and environmental isolates of Aspergillus fumigatus.
    Infect Immun. 1997 Aug;65(8):3080-5 PMID: 9234757
  86. A set of electrophoretic molecular markers for strain typing and population genetic studies of Histoplasma capsulatum.
    Electrophoresis. 1997 Jun;18(7):1047-53 PMID: 9237553
  87. Molecular markers reveal differentiation among isolates of Coccidioides immitis from California, Arizona and Texas.
    Mol Ecol. 1997 Aug;6(8):781-6 PMID: 9262014
  88. Molecular epidemiology of Cryptococcus neoformans in Brazil and the United States: evidence for both local genetic differences and a global clonal population structure.
    J Clin Microbiol. 1997 Sep;35(9):2243-51 PMID: 9276395
  89. Parity among the randomly amplified polymorphic DNA method, multilocus enzyme electrophoresis, and Southern blot hybridization with the moderately repetitive DNA probe Ca3 for fingerprinting Candida albicans.
    J Clin Microbiol. 1997 Sep;35(9):2348-58 PMID: 9276415
  90. Molecular taxonomy and epidemiology of Blastomyces and Histoplasma species.
    Mycoses. 1997 Sep;40(3-4):69-81 PMID: 9375491
  91. Phylogenetic assessment of length variation at a microsatellite locus.
    Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10745-9 PMID: 9380705
  92. Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus.
    Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):388-93 PMID: 9419385
  93. Detecting recombination from gene trees.
    Mol Biol Evol. 1998 May;15(5):590-9 PMID: 9580989
Article Info
Journal
Clinical microbiology reviews
Abbr.
Clin Microbiol Rev
ISSN
0893-8512
Published
1999-01-00
Pages
126-46
Language
English
Region
United States
NLM ID
8807282
PMCID
PMC88910
Subset
IM
Analysis Services
Analysis Services

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