Parasex generates phenotypic diversity de novo and impacts drug resistance and virulence in candida albicans

Genetics

Volumn 207, Issue 3, 2017, Pages 1195-1211

  Hirakawa, Matthew P ^a   Chyou, Darius E ^a   Huang, Denis ^a   Slan, Aaron R ^a   Bennett, Richard J ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Aneuploidy; Antifungal; Fluconazole; Pathogenesis; Sexual reproduction

Indexed keywords

AMPHOTERICIN B; ANTIFUNGAL AGENT; CASPOFUNGIN; FLUCONAZOLE; FLUCYTOSINE; GENOMIC DNA; VORICONAZOLE;

ANEUPLOIDY; ARTICLE; BIOFILM; CANDIDA ALBICANS; CHROMOSOME LOSS; CONTROLLED STUDY; DRUG RESISTANCE; ENVIRONMENTAL STRESS; FLOW CYTOMETRY; FUNGAL VIRULENCE; GALLERIA MELLONELLA; GROWTH RATE; MATING; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PARASEXUAL PROGENY; PATHOGENESIS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROGENY; REPRODUCTION; SUPERNUMERARY CHROMOSOME; ANTIFUNGAL RESISTANCE; CANDIDA; CELL DIVISION; CYTOLOGY; DRUG EFFECTS; GENETIC VARIATION; GENETICS; PATHOGENICITY; PHENOTYPE; PLOIDY; VIRULENCE;

ANTIFUNGAL AGENTS; CANDIDA; CELL DIVISION; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; GENETIC VARIATION; PHENOTYPE; PLOIDIES; VIRULENCE;

EID: 85032940645     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.117.300295     Document Type: Article

References (106)

1. Alby, K., and R. J. Bennett, 2009 Stress-induced phenotypic switching in Candida albicans. Mol. Biol. Cell 20: 3178–3191.
2. Alby, K., and R. J. Bennett, 2010 Sexual reproduction in the Candida clade: cryptic cycles, diverse mechanisms, and alternative functions. Cell. Mol. Life Sci. 67: 3275–3285.
3. Alby, K., and R. J. Bennett, 2011 Interspecies pheromone signaling promotes biofilm formation and same-sex mating in Candida albicans. Proc. Natl. Acad. Sci. USA 108: 2510–2515.
4. Alby, K., D. Schaefer, and R. J. Bennett, 2009 Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460: 890–893.
5. Anderson, J. B., C. Wickens, M. Khan, L. E. Cowen, N. Federspiel et al., 2001 Infrequent genetic exchange and recombination in the mitochondrial genome of Candida albicans. J. Bacteriol. 183: 865–872.
6. Bennett, R. J., and A. D. Johnson, 2003 Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J. 22: 2505–2515.
7. Bennett, R. J., M. A. Uhl, M. G. Miller, and A. D. Johnson, 2003 Identification and characterization of a Candida albicans mating pheromone. Mol. Cell. Biol. 23: 8189–8201.
8. Bennett, R. J., M. G. Miller, P. R. Chua, M. E. Maxon, and A. D. Johnson, 2005 Nuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene. Mol. Microbiol. 55: 1046–1059.
9. Bennett, R. J., A. Forche, and J. Berman, 2014 Rapid mechanisms for generating genome diversity: whole ploidy shifts, aneuploidy, and loss of heterozygosity. Cold Spring Harb. Perspect. Med. 4: a019604.
10. Berman, J., 2016 Ploidy plasticity: a rapid and reversible strategy for adaptation to stress. FEMS Yeast Res. 16: pii: fow020.
11. Berman, J., and L. Hadany, 2012 Does stress induce (para)sex? Implications for Candida albicans evolution. Trends Genet. 28: 197–203.
12. Brennan, M., D. Y. Thomas, M. Whiteway, and K. Kavanagh, 2002 Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol. Med. Microbiol. 34: 153–157.
13. Burt, A., 2000 Perspective: sex, recombination, and the efficacy of selection–was Weismann right? Evolution 54: 337–351.
14. Butler, G., M. D. Rasmussen, M. F. Lin, M. A. Santos, S. Sakthikumar et al., 2009 Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657–662.
15. Calderone, R. A., and W. A. Fonzi, 2001 Virulence factors of Candida albicans. Trends Microbiol. 9: 327–335.
16. Cao, F., S. Lane, P. P. Raniga, Y. Lu, Z. Zhou et al., 2006 The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans. Mol. Biol. Cell 17: 295–307.
17. Chen, G., W. D. Bradford, C. W. Seidel, and R. Li, 2012a Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy. Nature 482: 246–250.
18. Chen, G., B. Rubinstein, and R. Li, 2012b Whole chromosome aneuploidy: big mutations drive adaptation by phenotypic leap. Bioessays 34: 893–900.
19. Chen, X., B. B. Magee, D. Dawson, P. T. Magee, and C. A. Kumamoto, 2004 Chromosome 1 trisomy compromises the virulence of Candida albicans. Mol. Microbiol. 51: 551–565.
20. Chibana, H., J. L. Beckerman, and P. T. Magee, 2000 Fine-resolution physical mapping of genomic diversity in Candida albicans. Genome Res. 10: 1865–1877.
21. Coste, A., V. Turner, F. Ischer, J. Morschhauser, A. Forche et al., 2006 A mutation in Tac1p, a transcription factor regulating CDR1 and CDR2, is coupled with loss of heterozygosity at chromosome 5 to mediate antifungal resistance in Candida albicans. Genetics 172: 2139–2156.
22. Cotter, G., S. Doyle, and K. Kavanagh, 2000 Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol. Med. Microbiol. 27: 163–169.
23. Dumitru, R., D. H. Navarathna, C. P. Semighini, C. G. Elowsky, R. V. Dumitru et al., 2007 In vivo and in vitro anaerobic mating in Candida albicans. Eukaryot. Cell 6: 465–472.
24. Dunkel, N., J. Blass, P. D. Rogers, and J. Morschhauser, 2008 Mutations in the multi-drug resistance regulator MRR1, followed by loss of heterozygosity, are the main cause of MDR1 overexpression in fluconazole-resistant Candida albicans strains. Mol. Microbiol. 69: 827–840.
25. Finkel, J. S., and A. P. Mitchell, 2011 Genetic control of Candida albicans biofilm development. Nat. Rev. Microbiol. 9: 109–118.
26. Forche, A., K. Alby, D. Schaefer, A. D. Johnson, J. Berman et al., 2008 The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 6: e110.
27. Ford, C. B., J. M. Funt, D. Abbey, L. Issi, C. Guiducci et al., 2015 The evolution of drug resistance in clinical isolates of Candida albicans. Elife 4: e00662.
28. Fox, E. P., C. K. Bui, J. E. Nett, N. Hartooni, M. C. Mui et al., 2015 An expanded regulatory network temporally controls Candida albicans biofilm formation. Mol. Microbiol. 96: 1226–1239.
29. Fuchs, B. B., J. Eby, C. J. Nobile, J. B. El Khoury, A. P. Mitchell et al., 2010a Role of filamentation in Galleria mellonella killing by Candida albicans. Microbes Infect. 12: 488–496.
30. Fuchs, B. B., E. O’Brien, J. B. Khoury, and E. Mylonakis, 2010b Methods for using Galleria mellonella as a model host to study fungal pathogenesis. Virulence 1: 475–482.
31. Gerstein, A. C., A. Rosenberg, I. Hecht, and J. Berman, 2016 diskImageR: quantification of resistance and tolerance to antimicrobial drugs using disk diffusion assays. Microbiology 162: 1059–1068.
32. Gerstein, A. C., H. Lim, J. Berman, and M. A. Hickman, 2017 Ploidy tug-of-war: evolutionary and genetic environments influence the rate of ploidy drive in a human fungal pathogen. Evolution 71: 1025–1038.
33. Goddard, M. R., H. C. Godfray, and A. Burt, 2005 Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434: 636–640.
34. Graser, Y., M. Volovsek, J. Arrington, G. Schonian, W. Presber et al., 1996 Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination. Proc. Natl. Acad. Sci. USA 93: 12473–12477.
35. Gudlaugsson, O., S. Gillespie, K. Lee, J. Vande Berg, J. Hu et al., 2003 Attributable mortality of nosocomial candidemia, revisited. Clin. Infect. Dis. 37: 1172–1177.
36. Guthrie, C., and G. R. Fink, 1991 Guide to yeast genetics and molecular biology. Methods Enzymol. 194: 1–863.
37. Hao, B., C. J. Clancy, S. Cheng, S. B. Raman, K. A. Iczkowski et al., 2009 Candida albicans RFX2 encodes a DNA binding protein involved in DNA damage responses, morphogenesis, and virulence. Eukaryot. Cell 8: 627–639.
38. Harrison, B. D., J. Hashemi, M. Bibi, R. Pulver, D. Bavli et al., 2014 A tetraploid intermediate precedes aneuploid formation in yeasts exposed to fluconazole. PLoS Biol. 12: e1001815.
39. Heckman, D. S., D. M. Geiser, B. R. Eidell, R. L. Stauffer, N. L. Kardos et al., 2001 Molecular evidence for the early colonization of land by fungi and plants. Science 293: 1129–1133.
40. Heitman, J., 2010 Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8: 86–99.
41. Heitman, J., 2015 Evolution of sexual reproduction: a view from the fungal kingdom supports an evolutionary epoch with sex before sexes. Fungal Biol. Rev. 29: 108–117.
42. Hickman, M. A., G. Zeng, A. Forche, M. P. Hirakawa, D. Abbey et al., 2013 The ‘obligate diploid’ Candida albicans forms mating-competent haploids. Nature 494: 55–59.
43. Hickman, M. A., C. Paulson, A. Dudley, and J. Berman, 2015 Parasexual ploidy reduction drives population heterogeneity through random and transient aneuploidy in Candida albicans. Genetics 200: 781–794.
44. Hirakawa, M. P., D. A. Martinez, S. Sakthikumar, M. Z. Anderson, A. Berlin et al., 2015 Genetic and phenotypic intra-species variation in Candida albicans. Genome Res. 25: 413–425.
45. Hull, C. M., R. M. Raisner, and A. D. Johnson, 2000 Evidence for mating of the “asexual” yeast Candida albicans in a mammalian host. Science 289: 307–310.
46. Jacobsen, I. D., 2014 Galleria mellonella as a model host to study virulence of Candida. Virulence 5: 237–239.
47. Jokela, J., M. F. Dybdahl, and C. M. Lively, 2009 The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. Am. Nat. 174 (Suppl. 1): S43–S53.
48. Jones, Jr., S. K., and R. J. Bennett, 2011 Fungal mating pheromones: choreographing the dating game. Fungal Genet. Biol. 48: 668–676.
49. Jones, T., N. A. Federspiel, H. Chibana, J. Dungan, S. Kalman et al., 2004 The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. USA 101: 7329–7334.
50. Kwon-Chung, K. J., and Y. C. Chang, 2012 Aneuploidy and drug resistance in pathogenic fungi. PLoS Pathog. 8: e1003022.
51. Langmead, B., and S. L. Salzberg, 2012 Fast gapped-read alignment with Bowtie 2. Nat. Methods 9: 357–359.
52. Lehtonen, J., M. D. Jennions, and H. Kokko, 2012 The many costs of sex. Trends Ecol. Evol. 27: 172–178.
53. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan et al., 2009 The sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.
54. Lively, C. M., 2010 A review of Red Queen models for the persistence of obligate sexual reproduction. J. Hered. 101(Suppl. 1): S13–S20.
55. Lockhart, S. R., R. Zhao, K. J. Daniels, and D. R. Soll, 2003 Alpha-pheromone-induced “shmooing” and gene regulation require white-opaque switching during Candida albicans mating. Eukaryot. Cell 2: 847–855.
56. MacCallum, D. M., L. Castillo, K. Nather, C. A. Munro, A. J. Brown et al., 2009 Property differences among the four major Candida albicans strain clades. Eukaryot. Cell 8: 373–387.
57. 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.
58. Magee, B. B., and P. T. Magee, 2000 Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science 289: 310–313.
59. Mayer, F. L., D. Wilson, and B. Hube, 2013 Candida albicans pathogenicity mechanisms. Virulence 4: 119–128.
60. McDonald, M. J., D. P. Rice, and M. M. Desai, 2016 Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531: 233–236.
61. Merlini, L., O. Dudin, and S. G. Martin, 2013 Mate and fuse: how yeast cells do it. Open Biol. 3: 130008.
62. Miller, M. G., and A. D. Johnson, 2002 White-opaque switching in Candida albicans is controlled by mating-type locus homeodo-main proteins and allows efficient mating. Cell 110: 293–302.
63. Morran, L. T., O. G. Schmidt, I. A. Gelarden, R. C. Parrish, II, and C. M. Lively, 2011 Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333: 216–218.
64. Morrow, C. A., and J. A. Fraser, 2013 Ploidy variation as an adaptive mechanism in human pathogenic fungi. Semin. Cell Dev. Biol. 24: 339–346.
65. Morschhauser, J., K. S. Barker, T. T. Liu, B. W. J. Bla, R. Homayouni et al., 2007 The transcription factor Mrr1p controls expression of the MDR1 efflux pump and mediates multidrug resistance in Candida albicans. PLoS Pathog. 3: e164.
66. Mukherjee, P. K., B. Sendid, G. Hoarau, J. F. Colombel, D. Poulain et al., 2015 Mycobiota in gastrointestinal diseases. Nat. Rev. Gastroenterol. Hepatol. 12: 77–87.
67. Neiman, A. M., 2011 Sporulation in the budding yeast Saccharo-myces cerevisiae. Genetics 189: 737–765.
68. Ni, M., M. Feretzaki, S. Sun, X. Wang, and J. Heitman, 2011 Sex in fungi. Annu. Rev. Genet. 45: 405–430.
69. Ni, M., M. Feretzaki, W. Li, A. Floyd-Averette, P. Mieczkowski et al., 2013 Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol. 11: e1001653.
70. Nobile, C. J., and A. D. Johnson, 2015 Candida albicans biofilms and human disease. Annu. Rev. Microbiol. 69: 71–92.
71. Nobile, C. J., E. P. Fox, J. E. Nett, T. R. Sorrells, Q. M. Mitrovich et al., 2012 A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126–138.
72. Noble, S. M., S. French, L. A. Kohn, V. Chen, and A. D. Johnson, 2010 Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42: 590–598.
73. Odds, F. C., M. E. Bougnoux, D. J. Shaw, J. M. Bain, A. D. Davidson et al., 2007 Molecular phylogenetics of Candida albicans. Eukaryot. Cell 6: 1041–1052.
74. Panwar, S. L., M. Legrand, D. Dignard, M. Whiteway, and P. T. Magee, 2003 MFalpha1, the gene encoding the alpha mating pheromone of Candida albicans. Eukaryot. Cell 2: 1350–1360.
75. Perepnikhatka, V., F. J. Fischer, M. Niimi, R. A. Baker, R. D. Cannon et al., 1999 Specific chromosome alterations in fluconazole-resistant mutants of Candida albicans. J. Bacteriol. 181: 4041– 4049.
76. Prasad, R., P. De Wergifosse, A. Goffeau, and E. Balzi, 1995 Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr. Genet. 27: 320–329.
77. Quinlan, A. R., and I. M. Hall, 2010 BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842.
78. Rancati, G., N. Pavelka, B. Fleharty, A. Noll, R. Trimble et al., 2008 Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 135: 879– 893.
79. Robinson, J. T., H. Thorvaldsdottir, W. Winckler, M. Guttman, E. S. Lander et al., 2011 Integrative genomics viewer. Nat. Biotechnol. 29: 24–26.
80. Rustchenko, E., 2007 Chromosome instability in Candida albicans. FEMS Yeast Res. 7: 2–11.
81. Sanglard, D., F. Ischer, M. Monod, and J. Bille, 1997 Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology 143: 405–416.
82. Santaguida, S., and A. Amon, 2015 Short- and long-term effects of chromosome mis-segregation and aneuploidy. Nat. Rev. Mol. Cell Biol. 16: 473–485.
83. Saville, S. P., A. L. Lazzell, C. Monteagudo, and J. L. Lopez-Ribot, 2003 Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2: 1053–1060.
84. Schonherr, F. A., F. Sparber, F. R. Kirchner, E. Guiducci, K. Trautwein-Weidner et al., 2017 The intraspecies diversity of C. albicans triggers qualitatively and temporally distinct host responses that determine the balance between commensalism and pathogenicity. Mucosal Immunol. 10: 1335–1350.
85. Selmecki, A., A. Forche, and J. Berman, 2006 Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367–370.
86. Selmecki, A., M. Gerami-Nejad, C. Paulson, A. Forche, and J. Berman, 2008 An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol. Microbiol. 68: 624–641.
87. Selmecki, A., A. Forche, and J. Berman, 2010 Genomic plasticity of the human fungal pathogen Candida albicans. Eukaryot. Cell 9: 991–1008.
88. 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.
89. Sudbery, P. E., 2011 Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9: 737–748.
90. Sun, S., and J. Heitman, 2011 Is sex necessary? BMC Biol. 9: 56.
91. Tan, Z., M. Hays, G. A. Cromie, E. W. Jeffery, A. C. Scott et al., 2013 Aneuploidy underlies a multicellular phenotypic switch. Proc. Natl. Acad. Sci. USA 110: 12367–12372.
92. Tavanti, A., N. A. Gow, M. C. Maiden, F. C. Odds, and D. J. Shaw, 2004 Genetic evidence for recombination in Candida albicans based on haplotype analysis. Fungal Genet. Biol. 41: 553–562.
93. Taylor, J. W., and M. L. Berbee, 2006 Dating divergences in the fungal tree of life: review and new analyses. Mycologia 98: 838– 849.
94. Thorvaldsdottir, H., J. T. Robinson, and J. P. Mesirov, 2013 Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14: 178–192.
95. Torres, E. M., N. Dephoure, A. Panneerselvam, C. M. Tucker, C. A. Whittaker et al., 2010 Identification of aneuploidy-tolerating mutations. Cell 143: 71–83.
96. Van der Auwera, G. A., M. O. Carneiro, C. Hartl, R. Poplin, G. Del Angel et al., 2013 From FastQ data to high confidence variant calls: the genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinformatics 43: 11.10.1–11.10.33.
97. van het Hoog, M., T. J. Rast, M. Martchenko, S. Grindle, D. Dignard et al., 2007 Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes. Genome Biol. 8: R52.
98. van Werven, F. J., and A. Amon, 2011 Regulation of entry into gametogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366: 3521–3531.
99. Walker, B. J., T. Abeel, T. Shea, M. Priest, A. Abouelliel et al., 2014 Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9: e112963.
100. Wertheimer, N. B., N. Stone, and J. Berman, 2016 Ploidy dynamics and evolvability in fungi. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371: 20150461.
101. Wirsching, S., S. Michel, and J. Morschhauser, 2000 Targeted gene disruption in Candida albicans wild-type strains: the role of the MDR1 gene in fluconazole resistance of clinical Candida albicans isolates. Mol. Microbiol. 36: 856–865.
102. Wisplinghoff, H., T. Bischoff, S. M. Tallent, H. Seifert, R. P. Wenzel et al., 2004 Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39: 309– 317.
103. Wu, W., S. R. Lockhart, C. Pujol, T. Srikantha, and D. R. Soll, 2007 Heterozygosity of genes on the sex chromosome regu- lates Candida albicans virulence. Mol. Microbiol. 64: 1587– 1604.
104. Yona, A. H., Y. S. Manor, R. H. Herbst, G. H. Romano, A. Mitchell et al., 2012 Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl. Acad. Sci. USA 109: 21010– 21015.
105. Zeng, G., Y. M. Wang, F. Y. Chan, and Y. Wang, 2014 One-step targeted gene deletion in Candida albicans haploids. Nat. Protoc. 9: 464–473.
106. Zhang, N., B. B. Magee, P. T. Magee, B. R. Holland, E. Rodrigues et al., 2015 Selective advantages of a parasexual cycle for the yeast Candida albicans. Genetics 200: 1117–1132.