Comparative genomics of serial isolates of cryptococcus neoformans reveals gene associated with carbon utilization and virulence

G3: Genes, Genomes, Genetics

Volumn 3, Issue 4, 2013, Pages 675-686

  Ormerod, Kate L ^a,b   Morrow, Carl A ^a,b   Chow, Eve W L ^a,b   Lee, I Russel ^a,b   Arras, Samantha D M ^a,b   Schirra, Horst Joachim ^a,b   Cox, Gary M ^a   Fries, Bettina C ^c,d   Fraser, James A ^e  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b Australian Centre for Ecogenomics   (Australia)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Department of Medicine Mycology Research Unit Duke University ^*  (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cryptococcosis; Fungal; Microevolution; Pathogenesis; Relapse

Indexed keywords

MELANIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AT RICH SEQUENCE; CARBON SOURCE; CARBON UTILIZATION; CHROMOSOME 12; CONTROLLED STUDY; COPY NUMBER VARIATION; CRYPTOCOCCUS NEOFORMANS; DELETION MUTANT; FUNGAL CAPSULE; FUNGAL GENOME; FUNGAL VIRULENCE; GENE DELETION; GENE SEQUENCE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION;

ANIMALIA; FILOBASIDIELLA NEOFORMANS; MURINAE;

EID: 84878542791     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.005660     Document Type: Article

References (67)

1. Albers, C. A., G. Lunter, D. G. MacArthur, G. McVean, W. H. Ouwehand et al., 2011 Dindel: Accurate indel calls from short-read data. Genome Res. 21: 961-973.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, 1990 Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Brenner, S., 1974 Genetics of Caenorhabditis elegans. Genetics 77: 71-94.
4. Bubb, W. A., L. C. Wright, M. Cagney, R. T. Santangelo, T. C. Sorrell et al., 1999 Heteronuclear NMR studies of metabolites produced by Cryptococcus neoformans in culture media: Identification of possible virulence factors. Magn. Reson. Med. 42: 442-453.
5. Chen, K., J. W. Wallis, M. D. McLellan, D. E. Larson, J. M. Kalicki et al., 2009 BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nat. Methods 6: 677-681.
6. Cheon, S. A., K.-W. Jung, Y.-L. Chen, J. Heitman, Y.-S. Bahn et al., 2011 Unique evolution of the UPR pathway with a novel bZIP transcription factor, Hxl1, for controlling pathogenicity of Cryptococcus neoformans. PLoS Pathog. 7: e1002177.
7. Chu, Z., J. Li, M. Eshaghi, R. K. M. Karuturi, K. Lin et al., 2007 Adaptive expression responses in the Pol-g null strain of S. pombe depleted of mitochondrial genome. BMC Genomics 8: 323.
8. Chun, C. D., O. W. Liu, and H. D. Madhani, 2007 A link between virulence and homeostatic responses to hypoxia during infection by the human fungal pathogen Cryptococcus neoformans. PLoS Pathog. 3: 225-238.
9. Clancy, C. J., M. H. Nguyen, R. Alandoerffer, S. J. Cheng, K. Iczkowski et al., 2006 Cryptococcus neoformans var. grubii isolates recovered from persons with AIDS demonstrate a wide range of virulence during murine meningoencephalitis that correlates with the expression of certain virulence factors. Microbiology-Sgm 152: 2247-2255.
10. Cox, G. M., J. Mukherjee, G. T. Cole, A. Casadevall, and J. R. Perfect, 2000 Urease as a virulence factor in experimental cryptococcosis. Infect. Immun. 68: 443-448.
11. Desnos-Ollivier, M., S. Patel, A. R. Spaulding, C. Charlier, D. Garcia-Hermoso et al., 2010 Mixed infections and in vivo evolution in the human fungal pathogen Cryptococcus neoformans. Mbio 1: e00091-e10.
12. Dunham, M. J., H. Badrane, T. Ferea, J. Adams, P. O. Brown et al., 2002 Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99: 16144-16149.
13. Forche, A., D. Abbey, T. Pisithkul, M. A. Weinzierl, T. Ringstrom et al., 2011 Stress alters rates and types of loss of heterozygosity in Candida albicans. Mbio 2: e00129-e11.
14. Forche, A., P. T. Magee, A. Selmecki, J. Berman, and G. May, 2009 Evolution in Candida albicans populations during a single passage through a mouse host. Genetics 182: 799-811.
15. Foury, F., 1989 Cloning and sequencing of the nuclear gene MIP1 encoding the catalytic subunit of the yeast mitochondrial DNA polymerase. J. Biol. Chem. 264: 20552-20560.
16. Fraser, J. A., J. C. Huang, R. Pukkila-Worley, J. A. Alspaugh, T. G. Mitchell et al., 2005 Chromosomal translocation and segmental duplication in Cryptococcus neoformans. Eukaryot. Cell 4: 401-406.
17. Fraser, J. A., R. L. Subaran, C. B. Nichols, and J. Heitman, 2003 Recapitulation of the sexual cycle of the primary fungal pathogenCryptococcus neoformans var. gattii: Implications for an outbreak on Vancouver Island, Canada. Eukaryot. Cell 2: 1036-1045.
18. Fries, B.C., F. Y. Chen, B. P.Currie, andA.Casadevall, 1996 Karyotype instability in Cryptococcus neoformans infection. J. Clin. Microbiol. 34: 1531-1534.
19. Garcia-Hermoso, D., G. Janbon, and F. Dromer, 1999 Epidemiological evidence for dormant Cryptococcus neoformans infection. J. Clin. Microbiol. 37: 3204-3209.
20. Goodwin, T. J. D., and R. T. M. Poulter, 2001 The diversity of retrotransposons in the yeast Cryptococcus neoformans. Yeast 18: 865-880.
21. Gresham, D., M. M. Desai, C. M. Tucker, H. T. Jenq, D. A. Pai et al., 2008 The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4: e1000303.
22. Himmelreich, U., T. E. Dzendrowskyj, C. Allen, S. Dowd, R. Malik et al., 2001 Cryptococcomas distinguished from gliomas with MR spectroscopy: An experimental rat and cell culture study. Radiology 220: 122-128.
23. Hoboth, C., R. Hoffmann, A. Eichner, C. Henke, S. Schmoldt et al., 2009 Dynamics of adaptive microevolution of hypermutable Pseudomonas aeruginosa during chronic pulmonary infection in patients with cystic fibrosis. J. Infect. Dis. 200: 118-130.
24. Hu, G., P.-Y. Cheng, A. Sham, J. R. Perfect, and J. W. Kronstad, 2008 Metabolic adaptation in Cryptococcus neoformans during early murine pulmonary infection. Mol. Microbiol. 69: 1456-1475.
25. Hu, G., J. Wang, J. Choi, W. Jung, I. Liu et al., 2011 Variation in chromosome copy number influences the virulence of Cryptococcus neoformans and occurs in isolates from AIDS patients. BMC Genomics 12: 526.
26. Jain, N., B. L. Wickes, S. A. Keller, J. Fu, A. Casadevall et al., 2005 Molecular epidemiology of clinical Cryptococcus neoformans strains from India. J. Clin. Microbiol. 43: 5733-5742.
27. Kellis, M., B. W. Birren, and E. S. Lander, 2004 Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
28. Kennemann, L., X. Didelot, T. Aebischer, S. Kuhn, B. Drescher et al., 2011 Helicobacter pylori genome evolution during human infection. Proc. Natl. Acad. Sci. USA 108: 5033-5038.
29. Kortschak, R. D., P. W. Tucker, and R. Saint, 2000 ARID proteins come in from the desert. Trends Biochem. Sci. 25: 294-299.
30. Lee, I. R., E. W. L. Chow, C. A. Morrow, J. T. Djordjevic, and J. A. Fraser, 2011 Nitrogen metabolite repression of metabolism and virulence in the human fungal pathogen Cryptococcus neoformans. Genetics 188: 309- 323.
31. Lengeler, K. B., P. Wang, G. M. Cox, J. R. Perfect, and J. Heitman, 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. USA 97: 14455-14460.
32. Litvintseva, A. P., R. Thakur, R. Vilgalys, and T. G. Mitchell, 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.
33. Loftus, B. J., E. Fung, P. Roncaglia, D. Rowley, P. Amedeo et al., 2005 The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307: 1321-1324.
34. Lynch, M., W. Sung, K. Morris, N. Coffey, C. R. Landry et al., 2008 A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl. Acad. Sci. USA 105: 9272-9277.
35. Magditch, D. A., T.-B. Liu, C. Xue, and A. Idnurm, 2012 DNA mutations mediate microevolution between host-adapted forms of the pathogenic fungus Cryptococcus neoformans. PLoS Pathog. 8: e1002936.
36. McDade, H. C., and G. M. Cox, 2001 A new dominant selectable marker for use in Cryptococcus neoformans. Med. Mycol. 39: 151-154.
37. Minning, T. A., D. B. Weatherly, S. Flibotte, and R. L. Tarleton, 2011 Widespread, focal copy number variations (CNV) and whole chromosome aneuploidies in Trypanosoma cruzi strains revealed by array comparative genomic hybridization. BMC Genomics 12: 139.
38. Morrow, C. A., I. R. Lee, E. W. L. Chow, K. L. Ormerod, A. Goldinger et al., 2012 A unique chromosomal rearrangement in the Cryptococcus neoformans var. grubii type strain enhances key phenotypes associated with virulence. mBio 3: e00310-11.
39. Mortensen, K. L., R. H. Jensen, H. K. Johansen, M. Skov, T. Pressler et al., 2011 Aspergillus species and other molds in respiratory samples from patients with cystic fibrosis: a laboratory-based study with focus on Aspergillus fumigatus azole resistance. J. Clin. Microbiol. 49: 2243-2251.
40. Mylonakis, E., F. M. Ausubel, J. R. Perfect, J. Heitman, and S. B. Calderwood, 2002 Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc. Natl. Acad. Sci. USA 99: 15675- 15680.
41. Noverr, M. C., P. R. Williamson, R. S. Fajardo, and G. B. Huffnagle, 2004 CNLAC1 is required for extrapulmonary dissemination of Cryptococcus neoformans but not pulmonary persistence. Infect. Immun. 72: 1693-1699.
42. Ohno, S., 1970 Evolution by Gene Duplication. Springer, New York.
43. Park, B. J., K. A. Wannemuehler, B. J. Marston, N. Govender, P. G. Pappas et al., 2009 Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
44. Patsialou, A., D. Wilsker, and E. Moran, 2005 DNA-binding properties of ARID family proteins. Nucleic Acids Res. 33: 66-80.
45. Pavelka, N., G. Rancati, J. Zhu, W. D. Bradford, A. Saraf et al., 2010 Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468: 321-325.
46. Pereira, C. B., F. L. Bueno, A. L. T. Dias, M. Brigagao, C. R. Paula et al., 2009 Evaluation of laccases and melanization in clinical and environmental Cryptococcus neoformans samples by non-denaturing PAGE. J. Med. Microbiol. 58: 563-566.
47. Perfect, J. R., S. D. R. Lang, and D. T. Durack, 1980 Chronic cryptococcal meningitis: A new experimental model in rabbits. Am. J. Pathol. 101: 177-193.
48. Petzold, E. W., U. Himmelreich, E. Mylonakis, T. Rude, D. Toffaletti et al., 2006 Characterization and regulation of the trehalose synthesis pathway and its importance in the pathogenicity of Cryptococcus neoformans. Infect. Immun. 74: 5877-5887.
49. Pitkin, J. W., D. G. Panaccione, and J. D. Walton, 1996 A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum. Microbiology-Uk 142: 1557-1565.
50. Polakova, S., C. Blume, J. A. Zarate, M. Mentel, D. Jorck-Ramberg et al., 2009 Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc. Natl. Acad. Sci. USA 106: 2688-2693.
51. Selmecki, A., A. Forche, and J. Berman, 2006 Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367- 370.
52. Selmecki, A., A. Forche, and J. Berman, 2010 Genomic plasticity of the human fungal pathogen Candida albicans. Eukaryot. Cell 9: 991-1008.
53. Selmecki, A. M., K. Dulmage, L. E. Cowen, J. B. Anderson, and J. Berman, 2009 Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genet. 5: e1000705.
54. Sionov, E., H. Lee, Y. C. Chang, and K. J. Kwon-Chung, 2010 Cryptococcus neoformans overcomes stress of azole drugs by formation of disomy in specific multiple chromosomes. PLoS Pathog. 6: e1000848.
55. Slot, J. C., and A. Rokas, 2010 Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc. Natl. Acad. Sci. USA 107: 10136-10141.
56. Smit, A. F. A., R. Hubley, and P. Green, 1996-2010 RepeatMasker Open- 3.0. Available at: http://www.repeatmasker.org/.
57. Smith, E. E., D. G. Buckley, Z. N. Wu, C. Saenphimmachak, L. R. Hoffman et al., 2006 Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 103: 8487- 8492.
58. Southern, E., 2006 Southern blotting. Nat. Protoc. 1: 518-525.
59. Spitzer, E. D., S. G. Spitzer, L. F. Freundlich, and A. Casadevall, 1993 Persistence of initial infection in recurrent Cryptococcus neoformans meningitis. Lancet 341: 595-596.
60. Stukenbrock, E. H., F. G. Jorgensen, M. Zala, T. T. Hansen, B. A. McDonald et al., 2010 Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genet. 6: 12.
61. Sudarsanam, P., and F.Winston, 2000 The Swi/Snf family: nucleosome-remodeling complexes and transcriptional control. Trends Genet. 16: 345-351.
62. Torres, E. M., T. Sokolsky, C. M. Tucker, L. Y. Chan, M. Boselli et al., 2007 Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924.
63. Ubeda, J.-M., D. Legare, F. Raymond, A. A. Ouameur, S. Boisvert et al., 2008 Modulation of gene expression in drug resistant Leishmania is associated with gene amplification, gene deletion and chromosome aneuploidy. Genome Biol. 9: R115.
64. Wang, J. M., C. G. Mullighan, J. Easton, S. Roberts, S. L. Heatley et al., 2011 CREST maps somatic structural variation in cancer genomes with base-pair resolution. Nat. Methods 8: 652-654.
65. Waterman, S. R., M. Hacham, G. Hu, X. Zhu, Y.-D. Park et al., 2007 Role of a CUF1/CTR4 copper regulatory axis in the virulence of Cryptococcus neoformans. J. Clin. Invest. 117: 794-802.
66. Wilder, J. A., G. K. Olson, Y. C. Chang, K. J. Kwon-Chung, and M. F. Lipscomb, 2002 Complementation of a capsule deficient Cryptococcus neoformans with CAP64 restores virulence in a murine lung infection. Am. J. Respir. Cell Mol. Biol. 26: 306-314.
67. Wilsker, D., L. Probst, H. M. Wain, L. Maltais, P. W. Tueker et al., 2005 Nomenclature of the ARID family of DNA-binding proteins. Genomics 86: 242-251.