Microevolution of cryptococcus neoformans driven by massive tandem gene amplification

Molecular Biology and Evolution

Volumn 29, Issue 8, 2012, Pages 1987-2000

  Chow, Eve W L ^a   Morrow, Carl A ^a   Djordjevic, Julianne T ^b   Wood, Ian A ^a   Fraser, James A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

amplification; Cryptococcus neoformans; subtelomere

Indexed keywords

ARSENITE EFFLUX TRANSPORTER 3; CARRIER PROTEIN; NUCLEOTIDE; RIBOSOME DNA; UNCLASSIFIED DRUG;

AMPLICON; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CHROMOSOME 3; CLADISTICS; CONTROLLED STUDY; COPY NUMBER VARIATION; CRYPTOCOCCUS NEOFORMANS; ENVIRONMENTAL STRESS; FUNGAL GENOME; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS ISOLATION; GENE AMPLIFICATION; GENE DUPLICATION; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOUSE; NONHUMAN; SACCHAROMYCES CEREVISIAE; TELOMERE;

ANIMALS; ARSENITES; CHROMOSOMES, FUNGAL; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DISEASE MODELS, ANIMAL; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE AMPLIFICATION; GENE DELETION; GENE DOSAGE; GENES, FUNGAL; HUMANS; MICE; MICE, INBRED BALB C; MICROBIAL SENSITIVITY TESTS; PHYLOGENY; TELOMERE;

FILOBASIDIELLA NEOFORMANS; FUNGI; PROTISTA; SACCHAROMYCES CEREVISIAE;

EID: 84864642785     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss066     Document Type: Article

References (89)

1. Adams J, Puskas-Rozsa S, Simlar J, Wilke CM. 1992. Adaptation and major chromosomal changes in populations of Saccharomyces cerevisiae. Curr Genet. 22:13-19.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
3. Bergthorsson U, Andersson DI, Roth JR. 2007. Ohno's dilemma: evolution of new genes under continuous selection. Proc Natl Acad Sci U S A. 104:17004-17009.
4. Bethea EK, Carver BJ, Montedonico AE, Reynolds TB. 2010. The inositol regulon controls viability in Candida glabrata. Microbiology 156:452-462.
5. Blasi E, Brozzetti A, Francisci D, Neglia R, Cardinali G, Bistoni F, Vidotto V, Baldelli F. 2001. Evidence of microevolution in a clinical case of recurrent Cryptococcus neoformans meningoencephalitis. Eur J Clin Microbiol Infect Dis. 20:535-543.
6. Boekhout T, van Belkum A. 1997. Variability of karyotypes and RAPD types in genetically related strains of Cryptococcus neoformans. Curr Genet. 32:203-208.
7. Bosco G, Haber JE. 1998. Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150:1037-1047.
8. Broer S, Ji G, Broer A, Silver S. 1993. Arsenic efflux governed by the arsenic resistance determinant of Staphylococcus aureus plasmid pI258. J Bacteriol. 175:3480-3485.
9. Brown CA, Murray AW, Verstrepen KJ. 2010. Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol. 20:895-903.
10. Brown CJ, Todd KM, Rosenzweig RF. 1998. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol. 15:931-942.
11. Buchanan KL, Murphy JW. 1998. What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis. 4:71-83.
12. Casadevall A. 1998. Ecology of Cryptococcus neoformans. In: Casadevall A, Perfect JR, editors. Cryptococcus neoformans. Washington (DC): ASM Press. p. 41-70.
13. Chen YL, Kauffman S, Reynolds TB. 2008. Candida albicans uses multiple mechanisms to acquire the essential metabolite inositol during infection. Infect Immun. 76:2793-2801.
14. Chikamori M, Fukushima K. 2005. A new hexose transporter from Cryptococcus neoformans: molecular cloning and structural and functional characterization. Fungal Genet Biol. 42:646-655.
15. Church GM, Gilbert W. 1984. Genomic sequencing. Proc Natl Acad Sci U S A. 81:1991-1995.
16. Clinical and Laboratory Standards Institute. 2002. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved Standard-second edition. Wayne (PA): Clinical and Laboratory Standards Institute.
17. Dabbs ER, Sole GJ. 1988. Plasmid-borne resistance to arsenate, arsenite, cadmium, and chloramphenicol in a Rhodococcus species. Mol Gen Genet. 211:148-154.
18. Davidson RC, Cruz MC, Sia RA, Allen B, Alspaugh JA, Heitman J. 2000. Gene disruption by biolistic transformation in serotype D strains of Cryptococcus neoformans. Fungal Genet Biol. 29:38-48.
19. De Bruin D, Lanzer M, Ravetch JV. 1994. The polymorphic subtelomeric regions of Plasmodium falciparum chromosomes contain arrays of repetitive sequence elements. Proc Natl Acad Sci U S A. 91:619-623.
20. De Las Penas A, Pan SJ, Castano I, Alder J, Cregg R, Cormack BP. 2003. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1-and SIR-dependent transcriptional silencing. Genes Dev. 17:2245-2258.
21. Desnos-Ollivier M, Patel S, Spaulding AR, Charlier C, Garcia-Hermoso D, Nielsen K, Dromer F. 2010. Mixed infections and in vivo evolution in the human fungal pathogen Cryptococcus neoformans. MBio 1(1):e00091-10.
22. D'Souza CA, Kronstad JW, Taylor G, et al. (38 co-authors). 2011. Genome variation in Cryptococcus gattii, an emerging pathogen of immunocompetent hosts. MBio 2(1):e00342-10.
23. Fan C, Zhang Y, Yu Y, Rounsley S, Long M, Wing RA. 2008. The subtelomere of Oryza sativa chromosome 3 short arm as a hot bed of new gene origination in rice. Mol Plant. 1:839-850.
24. Farman ML. 2007. Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it. FEMS Microbiol Lett. 273:125-132.
25. Farman ML, Leong SA. 1995. Genetic and physical mapping of telomeres in the rice blast fungus, Magnaporthe grisea. Genetics 140:479-492.
26. Fischer G, James SA, Roberts IN, Oliver SG, Louis EJ. 2000. Chromosomal evolution in Saccharomyces. Nature 405:451-454.
27. Fleig U, Beinhauer JD, Hegemann JH. 1995. Functional selection for the centromere DNA from yeast chromosome VIII. Nucleic Acids Res. 23:922-924.
28. Flint J, Bates GP, Clark K, Dorman A, Willingham D, Roe BA, Micklem G, Higgs DR, Louis EJ. 1997. Sequence comparison of human and yeast telomeres identifies structurally distinct subtelomeric domains. Hum Mol Genet. 6:1305-1313.
29. Fraser JA, Giles SS, Wenink EC, et al. (8 co-authors). 2005. Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437:1360-1364.
30. Fraser JA, Huang JC, Pukkila-Worley R, Alspaugh JA, Mitchell TG, Heitman J. 2005. Chromosomal translocation and segmental duplication in Cryptococcus neoformans. Eukaryot Cell. 4:401-406.
31. Fraser JA, Subaran RL, Nichols CB, Heitman J. 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.
32. Fries BC, Chen F, Currie BP, Casadevall A. 1996. Karyotype instability in Cryptococcus neoformans infection. J Clin Microbiol. 34:1531-1534.
33. Ganley AR, Ide S, Saka K, Kobayashi T. 2009. The effect of replication initiation on gene amplification in the rDNA and its relationship to aging. Mol Cell. 35:683-693.
34. Ghannoum MA, Ibrahim AS, Fu Y, Shafiq MC, Edwards JE Jr, Criddle RS. 1992. Susceptibility testing of Cryptococcus neoformans: a microdilution technique. J Clin Microbiol. 30:2881-2886.
35. Ghosh M, Shen J, Rosen BP. 1999. Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 96:5001-5006.
36. Giaever G, Chu AM, Ni L, et al. (70 co-authors). 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
37. Haber JE, Debatisse M. 2006. Gene amplification: yeast takes a turn. Cell 125:1237-1240.
38. Haber JE, Ira G, Malkova A, Sugawara N. 2004. Repairing a doublestrand chromosome break by homologous recombination: revisiting Robin Holliday's model. Philos Trans R Soc Lond B Biol Sci. 359:79-86.
39. Hastings PJ. 2007. Adaptive amplification. Crit Rev Biochem Mol Biol. 42:271-283.
40. Hegemann JH, Fleig UN. 1993. The centromere of budding yeast. Bioessays 15:451-460.
41. Hosiner D, Lempiainen H, Reiter W, Urban J, Loewith R, Ammerer G, Schweyen R, Shore D, Schuller C. 2009. Arsenic toxicity to Saccharomyces cerevisiae is a consequence of inhibition of the TORC1 kinase combined with a chronic stress response. Mol Biol Cell. 20:1048-1057.
42. Ibeas JI, Jimenez J. 1996. Genomic complexity and chromosomal rearrangements in wine-laboratory yeast hybrids. Curr Genet. 30:410-416.
43. Idnurm A, Reedy JL, Nussbaum JC, Heitman J. 2004. Cryptococcus neoformans virulence gene discovery through insertional mutagenesis. Eukaryot Cell. 3:420-429.
44. Jain N, Guerrero A, Fries BC. 2006. Phenotypic switching and its implications for the pathogenesis of Cryptococcus neoformans. FEMS Yeast Res. 6:480-488.
45. Jain N, Wickes BL, Keller SM, Fu J, Casadevall A, Jain P, Ragan MA, Banerjee U, Fries BC. 2005. Molecular epidemiology of clinical Cryptococcus neoformans strains from India. J Clin Microbiol. 43:5733-5742.
46. Kavanaugh LA, Fraser JA, Dietrich FS. 2006. Recent evolution of the human pathogen Cryptococcus neoformans by intervarietal transfer of a 14-gene fragment. Mol Biol Evol. 23:1879-1890.
47. Killick R, Eckley IA. Forthcoming. Changepoint: an R package for changepoint analysis. Killick R, Fearnhead P, Eckley IA. 2011. Optimal detection of changepoints with a linear computational cost. IoP Publishing. Advance Access published January 2011, arXiv 1101.1438v2.
48. Koszul R, Caburet S, Dujon B, Fischer G. 2004. Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. EMBO J. 23:234-243.
49. Kuo HF, Olsen KM, Richards EJ. 2006. Natural variation in a subtelomeric region of Arabidopsis: implications for the genomic dynamics of a chromosome end. Genetics 173:401-417.
50. Kwon-Chung JK. 1986. Encapsulation and melanin formation as indicators of virulence in Cryptococcus neoformans. Infect Immun. 51:218-223.
51. Kwon-Chung KJ, Wickes BL, Stockman L, Roberts GD, Ellis D, Howard DH. 1992. Virulence, serotype, and molecular characteristics of environmental strains of Cryptococcus neoformans var. gattii. Infect Immun. 60:1869-1874.
52. Lengeler KB, Wang P, Cox GM, Perfect JR, Heitman J. 2000. Identification of the MATa mating-type locus of Cryptococcus neoformans reveals a serotype A MATa strain thought to have been extinct. Proc Natl Acad Sci U S A. 97:14455-14460.
53. Litvintseva AP, Kestenbaum L, Vilgalys R, Mitchell TG. 2005. Comparative analysis of environmental and clinical populations of Cryptococcus neoformans. J Clin Microbiol. 43:556-564.
54. Litvintseva AP, Marra RE, Nielsen K, Heitman J, Vilgalys R, Mitchell TG. 2003. Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot Cell. 2:1162-1168.
55. Litvintseva AP, Thakur R, Vilgalys R, Mitchell TG. 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.
56. Liu Z, Boles E, Rosen BP. 2004. Arsenic trioxide uptake by hexose permeases in Saccharomyces cerevisiae. J Biol Chem. 279: 17312-17318.
57. Loftus BJ, Fung E, Roncaglia P, et al. (51 co-authors). 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:1321-1324.
58. Louis EJ. 1995. The chromosome ends of Saccharomyces cerevisiae. Yeast 11:1553-1573.
59. Maciaszczyk-Dziubinska E, Migdal I, Migocka M, Bocer T, Wysocki R. 2010. The yeast aquaglyceroporin Fps1p is a bidirectional arsenite channel. FEBS Lett. 584:726-732.
60. Marra RE, Huang JC, Fung E, Nielsen K, Heitman J, Vilgalys R, Mitchell TG. 2004. A genetic linkage map of Cryptococcus neoformans variety neoformans serotype D (Filobasidiella neoformans). Genetics 167:619-631.
61. McEachern MJ, Haber JE. 2006. Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem. 75:111-135.
62. Mizuno H, Wu J, Kanamori H, Fujisawa M, Namiki N, Saji S, Katagiri S, Katayose Y, Sasaki T, Matsumoto T. 2006. Sequencing and characterization of telomere and subtelomere regions on rice chromosomes 1S, 2S, 2L, 6L, 7S, 7L and 8S. Plant J. 46:206-217.
63. Morrow CA, Fraser JA. 2009. Sexual reproduction and dimorphism in the pathogenic basidiomycetes. FEMS Yeast Res. 9:161-177.
64. Mukhopadhyay R, Rosen BP. 1998. Saccharomyces cerevisiae ACR2 gene encodes an arsenate reductase. FEMS Microbiol Lett. 168:127-136.
65. Nielsen K, Cox GM, Wang P, Toffaletti DL, Perfect JR, Heitman J. 2003. Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and alpha isolates. Infect Immun. 71:4831-4841.
66. Ogihara F, Kitagaki H, Wang Q, Shimoi H. 2008. Common industrial sake yeast strains have three copies of the AQY1-ARR3 region of chromosome XVI in their genomes. Yeast 25:419-432.
67. Park BJ, Wannemuehler KA, Marston BJ, Govender N, Pappas PG, Chiller TM. 2009. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23:525-530.
68. Perfect JR. 2005. Cryptococcus neoformans: a sugar-coated killer with designer genes. FEMS Immunol Med Microbiol. 45:395-404.
69. Pitkin JW, Panaccione DG, Walton JD. 1996. A putative cyclic peptide efflux pump encoded by the TOXA gene of the plantpathogenic fungus Cochliobolus carbonum. Microbiology 142(6):1557-1565.
70. Price MS, Betancourt-Quiroz M, Price JL, Toffaletti DL, Vora H, Hu G, Kronstad JW, Perfect JR. 2011. Cryptococcus neoformans requires a functional glycolytic pathway for disease but not persistence in the host. MBio 2(3):e00103-11.
71. Pryde FE, Gorham HC, Louis EJ. 1997. Chromosome ends: all the same under their caps. Curr Opin Genet Dev. 7:822-828.
72. Reams AB, Neidle EL. 2004. Selection for gene clustering by tandem duplication. Annu Rev Microbiol. 58:119-142.
73. Rehmeyer C, Li W, Kusaba M, Kim YS, Brown D, Staben C, Dean R, Farman M. 2006. Organization of chromosome ends in the rice blast fungus, Magnaporthe oryzae. Nucleic Acids Res. 34:4685-4701.
74. Romero D, Palacios R. 1997. Gene amplification and genomic plasticity in prokaryotes. Annu Rev Genet. 31:91-111.
75. Rosen BP. 1995. Resistance mechanisms to arsenicals and antimonials. J Basic Clin Physiol Pharmacol. 6:251-263.
76. Rosen BP. 2002. Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol. 133:689-693.
77. Schildkraut E, Miller CA, Nickoloff JA. 2005. Gene conversion and deletion frequencies during double-strand break repair in human cells are controlled by the distance between direct repeats. Nucleic Acids Res. 33:1574-1580.
78. Steenbergen JN, Shuman HA, Casadevall A. 2001. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A. 98:15245-15250.
79. Sun S, Xu J. 2009. Chromosomal rearrangements between serotype A and D strains in Cryptococcus neoformans. PLoS One 4:e5524.
80. Thompson JD, Higgins DG, Gibson TJ. 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.
81. Wang Y, Liu TB, Delmas G, Park S, Perlin D, Xue C. 2011. Two major inositol transporters and their role in cryptococcal virulence. Eukaryot Cell. 10:618-628.
82. Watanabe T, Horiuchi T. 2005. A novel gene amplification system in yeast based on double rolling-circle replication. EMBO J. 24:190-198.
83. Winzeler EA, Castillo-Davis CI, Oshiro G, Liang D, Richards DR, Zhou Y, Hartl DL. 2003. Genetic diversity in yeast assessed with whole-genome oligonucleotide arrays. Genetics 163:79-89.
84. Winzeler EA, Shoemaker DD, Astromoff A, et al. (49 co-authors). 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906.
85. Wu C, Kim YS, Smith KM, Li W, Hood HM, Staben C, Selker EU, Sachs MS, Farman ML. 2009. Characterization of chromosome ends in the filamentous fungus Neurospora crassa. Genetics 181:1129-1145.
86. Wysocki R, Bobrowicz P, Ulaszewski S. 1997. The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J Biol Chem. 272:30061-30066.
87. Wysocki R, Chery CC, Wawrzycka D, Van Hulle M, Cornelis R, Thevelein JM, Tamas MJ. 2001. The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol Microbiol. 40:1391-1401.
88. Xu J, Vilgalys R, Mitchell TG. 2000. Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neoformans. Mol Ecol. 9:1471-1481.
89. Xue C, Liu T, Chen L, Li W, Liu I, Kronstad JW, Seyfang A, Heitman J. 2010. Role of an expanded inositol transporter repertoire in Cryptococcus neoformans sexual reproduction and virulence. MBio 1(1):e00084-10.