Whole genome analysis of 132 clinical Saccharomyces cerevisiae strains reveals extensive ploidy variation

G3: Genes, Genomes, Genetics

Volumn 6, Issue 8, 2016, Pages 2421-2434

  Zhu, Yuan O ^a,b   Sherlock, Gavin ^a   Petrov, Dmitri A ^a  

^a STANFORD UNIVERSITY   (United States)

^b GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

Adaptation; Aneuploidy; Ploidy; Population sequencing; Population structure

Indexed keywords

ANEUPLOIDY; ARTICLE; CHROMOSOME SIZE; COPY NUMBER VARIATION; FUNGAL GENE; FUNGAL STRAIN; GENE DOSAGE; GENE FREQUENCY; GENE LOSS; GENE SEQUENCE; GENETIC VARIATION; GENOME ANALYSIS; INTROGRESSION; NONHUMAN; PHYLOGENY; PICHIA KUDRIAVZEVII; PLOIDY; POINT MUTATION; POLYPLOIDY; POPULATION STRUCTURE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES PARADOXUS; TRIPLOIDY; ADAPTATION; CELL LINEAGE; CHROMOSOME; FUNGAL GENOME; GENETICS; GENOMICS; MUTATION; PATHOGENICITY; TETRAPLOIDY;

ADAPTATION, BIOLOGICAL; ANEUPLOIDY; CELL LINEAGE; CHROMOSOMES, FUNGAL; GENOME, FUNGAL; GENOMICS; MUTATION; POLYPLOIDY; SACCHAROMYCES CEREVISIAE; TETRAPLOIDY;

EID: 84983681720     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.116.029397     Document Type: Article

References (100)

1. Albertin, W., P. Marullo, M. Aigle, A. Bourgais, M. Bely et al., 2009 Evidence for autotetraploidy associated with reproductive isolation in Saccharomyces cerevisiae: towards a new domesticated species. J. Evol. Biol. 22: 2157-2170.
2. Aucott, J. N., J. Fayen, H. Grossnicklas, A. Morrissey, M. M. Lederman et al., 1990 Invasive infection with Saccharomyces cerevisiae: report of three cases and review. Rev. Infect. Dis. 12: 406-411.
3. Barrio, E., S. González, A. Arias, C. Belloch, and A. Querol, 2006 Molecular mechanisms involved in the adaptive evolution of industrial yeasts, pp. 153-174 in The Yeast Handbook, edited by Querol, A., and G. H. Fleet. Springer Verlag, Berlin, Germany.
4. Berman, J., 2016 Ploidy plasticity: a rapid and reversible strategy for adaptation to stress. FEMS Yeast Res. 16(3): abstract Available at http://femsyr.oxfordjournals.org/content/16/3/fow020.
5. Bidenne, C., B. Blondin, S. Dequin, and F. Vezinhet, 1992 Analysis of the chromosomal DNA polymorphism of wine strains of Saccharomyces cerevisiae. Curr. Genet. 22: 1-7.
6. Biggins, S., N. Bhalla, A. Chang, D. L. Smith, and A. W. Murray, 2001 Chromatid separation and segregation in the budding yeast Saccharomyces cerevisiae. Genetics 159(2): 453-470.
7. Blondin, B., S. Dequin, A. Querol, and J. L. Legras, 2009 Genome of Saccharomyces cerevisiae and related yeasts, pp. 361-378 in Biology of Microorganisms on Grapes, in Must and in Wine.19
8. Carbon, S., A. Ireland, C. J. Mungall, S. Q. Shu, B. Marshall et al., 2009 AmiGO: online access to ontology and annotation data. Bioinformatics 25(2): 288-289.
9. Carro, D., E. Bartra, and B. Pina, 2003 Karyotype rearrangements in a wine yeast strain by rad52-dependent and rad52-independent mechanisms. Appl. Environ. Microbiol. 69: 2161-2165.
10. Cassone, M., P. Serra, F. Mondello, A. Girolamo, S. Scafetti et al., 2003 Outbreak of Saccharomyces cerevisiae subtype boulardii fungemia in patients neighboring those treated with a probiotic preparation of the organism. J. Clin. Microbiol. 41(11): 5340-5343.
11. Cavalieri, D., P. E. McGovern, D. L. Hartl, R. Mortimer, and M. Polsinelli, 2003 Evidence for S. cerevisiae fermentation in ancient wine. J. Mol. Evol. 57: S226-S232.
12. Cheng, E., J. A. Vaisica, J. Ou, A. Baryshnikova, Y. Lu et al., 2012 Genome rearrangements caused by depletion of essential DNA replication proteins in Saccharomyces cerevisiae. Genetics 192(1): 147-160.
13. Cho, U. S., and S. C. Harrison, 2011 Ndc10 is a platform for inner kinetochore assembly in budding yeast. Nat. Struct. Mol. Biol. 19: 48-55.
14. Clemons, K. V., J. H. McCusker, R. W. Davis, and D. A. Stevens, 1994 Comparative pathogenesis of clinical and nonclinical isolates of Saccharomyces cerevisiae. J. Infect. Dis. 169: 859-867.
15. Clemons, K. V., L. C. Hanson, and D. A. Stevens, 1996 Colony phenotype switching in clinical and non-clinical isolates of Saccharomyces cerevisiae. J. Med. Vet. Mycol. 34: 259-264.
16. Coyle, S., and E. Kroll, 2008 Starvation induces genomic rearrangements and starvation-resilient phenotypes in yeast. Mol. Biol. Evol. 25: 310-318.
17. Cromie, G. A., and A. M. Dudley, 2015 Aneuploidy: tolerating tolerance. Curr. Biol. 25(17): R771-R773.
18. de Llanos, R., A. Querol, A. M. Planes, and M. T. Fernández-Espinar, 2004 Molecular characterization of clinical Saccharomyces cerevisiae isolates and their association with non-clinical strains. Syst. Appl. Microbiol. 27: 427-435.
19. de Llanos, R., M. T. Fernandez-Espinar, and A. Querol, 2006a A comparison of clinical and food Saccharomyces cerevisiae isolates on the basis of potential virulence factors. Antonie van Leeuwenhoek 90: 221-231.
20. de Llanos, R., A. Querol, J. Peman, M. Gobernado, and M. T. Fernández-Espinar, 2006b Food and probiotic strains from the Saccharomyces cerevisiae species as a possible origin of human systemic infections. Int. J. Food Microbiol. 110: 286-290.
21. de Llanos, R., S. Llopis, G. Molero, A. Querol, C. Gil et al., 2011 In vivo virulence of commercial Saccharomyces cerevisiae strains with pathogenicity-associated phenotypical traits. Int. J. Food Microbiol. 144(3): 393-399.
22. Dequin, S., and S. Casaregola, 2011 The genomes of fermentative Saccharomyces. C. R. Biol. 334: 687-693.
23. Dougherty, S. H., and R. L. Simmons, 1982 Postoperative peritonitis caused by Saccharomyces cerevisiae. Arch. Surg. 117: 248.
24. Doyle, M. G., L. K. Pickering, N. O'Brien, K. Hoots, and J. E. Benson, 1990 Saccharomyces cerevisiae infection in a patient with acquired immunodeficiency syndrome. Pediatr. Infect. Dis. J. 9: 850-851.
25. Dunn, B., C. Richter, D. J. Kvitek, T. Pugh, and G. Sherlock, 2012 Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res. 22(5): 908-924.
26. Enache-Angoulvant, A., and C. Hennequin, 2005 Invasive Saccharomyces infection: a comprehensive review. Nephrol. Dial. Transplant. 41(11): 1559-1568.
27. Erdem, H., M. Cetin, T. Timuroglu, A. Cetin, O. Yanar et al., 2003 Identification of yeasts in public hospital primary care patients with or without clinical vaginitis. Aust. N. Z. J. Obstet. Gynaecol. 43: 312-316.
28. Falush, D., M. Stephens, and J. K. Pritchard, 2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4): 1567-1587.
29. Falush, D., M. Stephens, and J. K. Pritchard, 2007 Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol. Ecol. Notes 7(4): 574-578.
30. Farrell, A. E., R. J. Plevin, B. T. Turner, A. D. Jones, M. O'Hare et al., 2006 Ethanol can contribute to energy and environmental goals. Science 311: 506-508.
31. Gasch, A. P., J. Hose, M. A. Newton, M. Sardi, M. Yong et al., 2016 Further support for aneuploid tolerance in wild yeast and effects of dosage compensation on gene copy-number evolution. eLife 5: e14409.
32. Gayevskiy, V., and M. R. Goddard, 2012 Geographic delineations of yeast communities and populations associated with vines and wines in New Zealand. ISME J. 6(7): 1281-1290 .10.1038/ismej.2011.195
33. Goddard, M. R., and D. Greig, 2015 Saccharomyces cerevisiae: a nomadic yeast with no niche? FEMS Yeast Res. 15(3): abstract Available at http://femsyr.oxfordjournals.org/content/15/3/fov009.
34. Goddard, M. R., N. Anfang, R. Y. Tang, R. C. Gardner, and C. Jun, 2010 A distinct population of Saccharomyces cerevisiae in New Zealand: evidence for local dispersal by insects and human-aided global dispersal in oak barrels. Environ. Microbiol. 12(1): 63-73.
35. Goh, P. Y., and J. V. Kilmartin, 1993 NDC10: A gene involved in chromosome segregation in Saccharomyces cerevisiae. J. Cell Biol. 121(3): 503-512.
36. Hennequin, C., C. Kauffmann-Lacroix, A. Jobert, J. P. Viard, C. Ricour et al., 2000 Possible role of catheters in Saccharomyces boulardii fungemia. Eur. J. Clin. Microbiol. Infect. Dis. 19: 16-20.
37. 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(3): 781-794.
38. 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(3): 413-425.
39. Hittinger, C. T., and S. B. Carroll, 2007 Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449: 677-681.
40. Hose, J., C. M. Yong, M. Sardi, A. Wang, M. A. Newton et al., 2015 Dosage compensation can buffer copy-number variation in wild yeast. eLife 4: e05462.
41. Hubisz, M. J., D. Falush, M. Stephens, and J. K. Pritchard, 2009 Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9(5): 1322-1332.
42. James, T. C., J. Usher, S. Campbell, and U. Bond, 2008 Lager yeast possess dynamic genomes that undergo rearrangements and amplification in response to stress. Curr. Genet. 3: 139-152.
43. Klingberg, T. D., U. Lesnik, N. Arneborg, P. Raspor, and L. Jespersen, 2008 Comparison of Saccharomyces cerevisiae strains of clinical and nonclinical origin by molecular typing and determination of putative virulence traits. FEMS Yeast Res. 8(4): 631-640.
44. Kumaran, R., S. Y. Yang, and J. Y. Leu, 2013 Characterization of chromosome stability in diploid, polyploid, and hybrid yeast cells. PLoS One 10.1371/journal.pone.0068094.
45. Lang, G. I., D. P. Rice, M. J. Hickman, E. Sodergren, G. M. Weinstock et al., 2013 Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571-574.
46. Legras, J.-L., D. Merdinoglu, J.-M. Cornuet, and F. Karst, 2007 Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol. Ecol. 16(10): 2091-2102.
47. Letunic, I. and P. Bork 2006 Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23(1): 127-128.20
48. Letunic, I. and P. Bork 2011 Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39(suppl 2): W475-W478.21
49. Lherm, T., C. Monet, B. Nougiere, M. Soulier, D. Larbi et al., 2002 Seven cases of fungemia with Saccharomyces boulardii in critically ill patients. Intensive Care Med. 28: 797-801.
50. Li, H., and R. Durbin, 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14): 1754-1760.
51. Li, R., Y. Li, X. Fang, H. Yang, J. Wang et al., 2009 SNP detection for massively parallel whole genome resequencing. Genome Res. 19(6): 1124-1132.
52. Liti, G., 2015 The natural history of model organisms: The fascinating and secret wild life of the budding yeast: S. cerevisiae. eLife 4: e05835.
53. Liti, G., D. M. Carter, A. M. Moses, J. Warringer, L. Parts et al., 2009 Population genomics of domestic and wild yeasts. Nature 458 (7236): 337-341.
54. Malgoire, J. Y., S. Bertout, F. Renaud, J. M. Bastide, and M. Mallié, 2005 Typing of Saccharomyces cerevisiae clinical strains by using microsatellite sequence polymorphism. J. Clin. Microbiol. 43(3): 1133-1137.
55. McCullough, M. J., K. V. Clemons, C. Farina, J. H. McCusker, and D. A. Stevens, 1998 Epidemiological investigation of vaginal Saccharomyces cerevisiae isolates by a genotypic method. J. Clin. Microbiol. 36: 557-562.
56. McCusker, J. H., K. V. Clemons, D. A. Stevens, and R. W. Davis, 1994 Saccharomyces cerevisiae virulence phenotype as determined with CD-1 mice is associated with the ability to grow at 42 degrees C and form pseudohyphae. Infect. Immun. 62(12): 5447-5455.
57. McGovern, P. E., U. Hartung, V. R. Badler, D. L. Glusker, and L. J. Exner, 1997 The beginnings of winemaking and viniculture in the ancient Near East and Egypt. Expedition 39: 3-21.
58. McGovern, P. E., J. Zhang, J. Tang, Z. Zhang, G. R. Hall et al., 2004 Fermented beverages of pre-and proto-historic China. Proc. Natl. Acad. Sci. USA 101: 17593-17598.
59. McKenna, A., M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis et al., 2010 The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20(1): 1297-1303.
60. McKenzie, D. A., M. Defernez, W. B. Dunn, M. Brown, L. J. Fuller et al., 2008 Relatedness of medically important strains of Saccharomyces cerevisiae as revealed by phylogenetics and metabolomics. Yeast 25(7): 501-512.
61. Muller, L. A., and J. H. McCusker, 2009a A multispecies-based taxonomic microarray reveals interspecies hybridization and introgression in Saccharomyces cerevisiae. FEMS Yeast Res. 9(1): 143-152.
62. Muller, L. A., and J. H. McCusker, 2009b Microsatellite analysis of genetic diversity among clinical and nonclinical Saccharomyces cerevisiae isolates suggests heterozygote advantage in clinical environments. Mol. Ecol. 18 (13): 2779-2786.
63. Muller, L. A., and J. H. McCusker, 2011 Nature and distribution of large sequence polymorphisms in Saccharomyces cerevisiae. FEMS Yeast Res. 11(7): 587-594.22
64. Muller, L. A., J. E. Lucas, D. R. Geogianna, and J. H. McCusker, 2011 Genomewide association analysis of clinical vs. nonclinical origin provides insights into Saccharomyces cerevisiae pathogenesis. Mol. Ecol. 20(19): 4085-4097.
65. Munoz, P., E. Bouza, M. Cuenca-Estrella, J. M. Eiros, M. J. Perez et al., 2005 Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin. Infect. Dis. 40: 1625-1634.
66. Mydlik, M., E. Tkacova, K. Szovenyiova, P. Mizla, and K. Derzsiova, 1996 Saccharomyces cerevisiae peritonitis complicating CAPD. Perit. Dial. Int. 16: 188.
67. Ouspenski, I. I., S. J. Elledge, and B. R. Brinkley, 1999 New yeast genes important for chromosome integrity and segregation identified by dosage effects on genome stability. Nucleic Acids Res. 27(15): 3001-3008.
68. 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(7321): 321-325.
69. Perapoch, J., A. M. Planes, A. Querol, V. López, I. Martínez-Bendayán et al., 2000 Fungemia with Saccharomyces cerevisiae in two newborns, only one of whom had been treated with Ultra-Levura. Eur. J. Clin. Microbiol. Infect. Dis. 19: 468-470.
70. Perez-Torrado, R., S. Llopis, L. Jespersen, T. Fernández-Espinar, A. Querol et al., 2012 Clinical Saccharomyces cerevisiae isolates cannot cross the epithelial barrier in vitro. Int. J. Food Microbiol. 157(1): 59-64.
71. Peter, J., and J. Schacherer, 2015 Population genomics of yeasts: towards a comprehensive view across a broad evolutionary scale. Yeast 10.1002/yea.3142.
72. Piarroux, R., L. Millon, K. Bardonnet, O. Vagner, and H. Koenig, 1999 Are live saccharomyces yeasts harmful to patients? Lancet 353: 1851-1852.
73. Posteraro, B., M. Sanguinetti, G. D'Amore, L. Masucci, G. Morace et al., 1999 Molecular and epidemiological characterization of vaginal Saccharomyces cerevisiae isolates. J. Clin. Microbiol. 37: 2230-2235.
74. Pritchard, J. K., M. Stephens, and P. Donnelly, 2000 Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
75. Querol, A., and U. Bond, 2009 The complex and dynamic genomes of industrial yeasts. FEMS Microbiol. Lett. 293: 1-10.
76. Rancati, G., and N. Pavelka, 2013 Karyotypic changes as drivers and catalyzers of cellular evolvability: a perspective from non-pathogenic yeasts. Semin. Cell Dev. Biol. 24(4): 332-338.
77. 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.
78. Reimand, J., T. Arak, and J. Vilo, 2011 g Profiler-a web server for functional interpretation of gene lists (2011 update). Nucleic Acids Res. 10.1093/nar/gkr378.
79. Salonen, J. H., M. D. Richardson, K. Gallacher, J. Issakainen, H. Helenius et al., 2000 Fungal colonization of haematological patients receiving cytotoxic chemotherapy: emergence of azole-resistant Saccharomyces cerevisiae. J. Hosp. Infect. 45: 293-301.
80. Samuel, D., 1996 Investigation of ancient Egyptian baking and brewing methods by correlative microscopy. Science 273: 488-490.
81. Schacherer, J., J. A. Shapiro, D. M. Ruderfer, and L. Kruglyak, 2009 Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458(7236): 342-345.
82. 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(10): e1000705.
83. Selmecki, A. M., Y. E. Maruvka, P. A. Richmond, M. Guillet, N. Shoresh et al., 2015 Polyploidy can drive rapid adaptation in yeast. Nature 519(7543): 349-352.
84. Sheppard, T. K., B. C. Hitz, S. R. Engel, G. Song, R. Balakrishnan et al., 2016 The Saccharomyces Genome Database Variant Viewer. Nucleic Acids Res. 44(D1): D698-D702.
85. Sicard, D., and J. L. Legras, 2011 Bread, beer and wine: yeast domestication in the Saccharomyces sensu stricto complex. C. R. Biol. 334(3): 229-236.
86. Smith, D., D. Metzgar, C. Wills, and J. Fierer, 2002 Fatal Saccharomyces cerevisiae aortic graft infection. J. Clin. Microbiol. 40(7): 2691-2692.
87. Stambuk, B. U., B. Dunn, S. L. Alves, Jr, E. H. Duval, and G. Sherlock, 2009 Industrial fuel ethanol yeasts contain adaptive copy number changes in genes involved in vitamin B1 and B6 biosynthesis. Genome Res. 19(12): 2271-2278.
88. Stirling, P. C., M. S. Bloom, T. Solanki-Patil, S. Smith, P. Sopahimalani et al., 2011 The complete spectrum of yeast chromosome instability genes identifies candidate CIN cancer genes and functional roles for ASTRA complex components. PLoS Genet. 10.1371/journal.pgen.1002057.
89. Strope, P. K., D. A. Skelly, S. G. Kozmin, G. Mahadevan, E. A. Stone et al., 2015 The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res. 25(5): 762-774.
90. Sunshine, A. B., C. Payen, G. T. Ong, I. Liachko, K. M. Tan et al., 2015 The fitness consequences of aneuploidy are driven by condition-dependent gene effects. PLoS Biol. 13(5): e1002155.
91. Thorburn, R. R., C. Gonzalez, G. A. Brar, S. Christen, T. M. Carlile et al., 2013 Aneuploid yeast strains exhibit defects in cell growth and passage through START. Mol. Biol. Cell 24(9): 1274-1289.
92. Waghmare, S. K., and C. V. Bruschi, 2005 Differential chromosome control of ploidy in the yeast Saccharomyces cerevisiae. Yeast 22(8): 625-639.
93. Wang, Q. M., W. Q. Liu, G. Liti, S. A. Wang, and F. Y. Bai, 2012 Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21(22): 5404-5417.
94. Wei, W., J. H.McCusker, R.W.Hyman, T. Jones, Y. Ning et al., 2007 Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc. Natl. Acad. Sci. USA 104: 12825-12830.
95. Wheeler, R. T., M. Kupiec, P. Magnelli, C. Abeijon, and G. R. Fink, 2003 A Saccharomyces cerevisiae mutant with increased virulence. Proc. Natl. Acad. Sci. USA 100: 2766-2770.
96. Whittaker, S. G., B. M. Rockmill, E. Blechl, D. H. Maloney, M. Resnick et al., 1988 The detection of mitotic and meiotic aneuploidy in yeast using a gene dosage selection system. Molecular & General Genetics: MGG 215(1): 10-18.
97. Zerva, L., R. J. Hollis, and M. A. Pfaller, 1996 In vitro susceptibility testing and DNA typing of Saccharomyces cerevisiae clinical isolates. J. Clin. Microbiol. 34: 3031-3034.
98. Zhu, J., N. Pavelka, W. D. Bradford, G. Rancati, and R. Li, 2012 Karyotypic determinants of chromosome instability in aneuploid budding yeast. PLoS Genet.
99. Zhu, Y. O., M. L. Siegal, D. W. Hall, and D. A. Petrov, 2014 Precise estimates of mutation rate and spectrum in yeast. Proc. Natl. Acad. Sci. USA 111(22): E2310-E2318.
100. Zörgö, E., K. Chwialkowska, A. B. Gjuvsland, E. Garré, P. Sunnerhagen et al., 2013 Evolutionary trade-offs between yeast ploidy states. PLoS Genet. 9(3): e1003388.