1887

Microbial Genomics logo

Volume 10, Issue 1

Population genomic analyses reveal high diversity, recombination and nosocomial transmission among () isolates causing invasive infections Open Access

Abstract

is a commensal yeast of the gastrointestinal tract and skin of humans. However, it causes opportunistic infections in immunocompromised patients, and is the second most common pathogen causing bloodstream infections. Although there are many studies on the epidemiology of infections, the fine- and large-scale geographical nature of remain incompletely understood. Here we investigated both the fine- and large-scale population structure of through genome sequencing of 80 clinical isolates obtained from six tertiary hospitals in Qatar and by comparing with global collections. Our fine-scale analyses revealed high genetic diversity within the Qatari population of and identified signatures of recombination, inbreeding and clonal expansion within and between hospitals, including evidence for nosocomial transmission among coronavirus disease 2019 (COVID-19) patients. In addition to signatures of recombination at the population level, both MATa and MATα alleles were detected in most hospitals, indicating the potential for sexual reproduction in clinical environments. Comparisons with global samples showed that the Qatari population was very similar to those from other parts of the world, consistent with the significant role of recent anthropogenic activities in shaping its population structure. Genome-wide association studies identified both known and novel genomic variants associated with reduced susceptibilities to fluconazole, 5-flucytosine and echinocandins. Together, our genomic analyses revealed the diversity, transmission patterns and antifungal drug resistance mechanisms of in Qatar as well as the relationships between Qatari isolates and those from other parts of the world.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antifungal susceptibility , candidaemia , comparative genomics , Middle East and nosocomial
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001179
2024-01-16
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/1/mgen001179.html?itemId=/content/journal/mgen/10.1099/mgen.0.001179&mimeType=html&fmt=ahah

References

  1. Fidel PL, Vazquez JA, Sobel JD. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin Microbiol Rev 1999; 12:80–96 [View Article] [PubMed]
     [Google Scholar]
  2. Xu J. Assessing global fungal threats to humans. mLife 2022; 1:223–240 [View Article]
     [Google Scholar]
  3. Ahmad KM, Kokošar J, Guo X, Gu Z, Ishchuk OP et al. Genome structure and dynamics of the yeast pathogen Candida glabrata. FEMS Yeast Res 2014; 14:529–535 [View Article] [PubMed]
     [Google Scholar]
  4. Guinea J. Global trends in the distribution of Candida species causing candidemia. Clin Microbiol Infect 2014; 20 Suppl 6:5–10 [View Article] [PubMed]
     [Google Scholar]
  5. Pfaller MA, Andes DR, Diekema DJ, Horn DL, Reboli AC et al. Epidemiology and outcomes of invasive candidiasis due to non-albicans species of Candida in 2,496 patients: data from the Prospective Antifungal Therapy (PATH) registry 2004-2008. PLoS One 2014; 9:e101510 [View Article] [PubMed]
     [Google Scholar]
  6. Khatib R, Johnson LB, Fakih MG, Riederer K, Briski L. Current trends in candidemia and species distribution among adults: Candida glabrata surpasses C. albicans in diabetic patients and abdominal sources. Mycoses 2016; 59:781–786 [View Article] [PubMed]
     [Google Scholar]
  7. Perlroth J, Choi B, Spellberg B. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol 2007; 45:321–346 [View Article] [PubMed]
     [Google Scholar]
  8. Kounatidis I, Ames L, Mistry R, Ho H-L, Haynes K et al. A host-pathogen interaction screen identifies ada2 as a mediator of Candida glabrata defenses against reactive oxygen species. G3 2018; 8:1637–1647 [View Article] [PubMed]
     [Google Scholar]
  9. McCarty TP, Pappas PG. Invasive candidiasis. Infect Dis Clin North Am 2016; 30:103–124 [View Article] [PubMed]
     [Google Scholar]
  10. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 2007; 20:133–163 [View Article] [PubMed]
     [Google Scholar]
  11. Pfaller MA, Messer SA, Moet GJ, Jones RN, Castanheira M. Candida bloodstream infections: comparison of species distribution and resistance to echinocandin and azole antifungal agents in Intensive Care Unit (ICU) and non-ICU settings in the SENTRY Antimicrobial Surveillance Program (2008-2009). Int J Antimicrob Agents 2011; 38:65–69 [View Article] [PubMed]
     [Google Scholar]
  12. Pfaller MA, Diekema DJ, Steele-Moore L, Denys G, Staley C et al. Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect 2004; 10 Suppl 1:11–23 [View Article] [PubMed]
     [Google Scholar]
  13. He C, Song Y, Chang XK. Pathogenicity and drug-resistance analysis of Candida glabrata in patients with oral candidiasis. Zhonghua Yi Xue Za Zhi 2020; 100:1778–1782 [View Article] [PubMed]
     [Google Scholar]
  14. Fan Y, Pan W, Wang G, Huang Y, Li Y et al. Isolated cutaneous granuloma caused by Candida glabrata: a rare case report and literature review. Mycopathologia 2018; 183:417–421 [View Article] [PubMed]
     [Google Scholar]
  15. Krishna Chaaithanya I, Mujumdar Y, Anwesh M, Aranha C. Novel genotypes of vaginal Candida glabrata isolates from premenopausal asymptomatic women with vulvovaginitis. Eur J Obstet Gynecol Reprod Biol 2022; 276:249–250 [View Article] [PubMed]
     [Google Scholar]
  16. Celik AD, Yulugkural Z, Kuloglu F, Akata F. Candida glabrata: etiologic agent of soft tissue abscess in a diabetic patient. Indian J Pathol Microbiol 2010; 53:590–591 [View Article] [PubMed]
     [Google Scholar]
  17. Fisher MC, Denning DW. The WHO fungal priority pathogens list as a game-changer. Nat Rev Microbiol 2023; 21:211–212 [View Article] [PubMed]
     [Google Scholar]
  18. Xu J, Boyd CM, Livingston E, Meyer W, Madden JF et al. Species and genotypic diversities and similarities of pathogenic yeasts colonizing women. J Clin Microbiol 1999; 37:3835–3843 [View Article] [PubMed]
     [Google Scholar]
  19. Hong J-M, Hu L-H, Zhong Q-S, Zhu L-C, Hang Y-P et al. Epidemiological characteristics and clinical features of patients infected with the COVID-19 virus in Nanchang, Jiangxi, China. Front Med 2020; 7:571069 [View Article] [PubMed]
     [Google Scholar]
  20. Kang MJ, Choi YS, Lee J, Shin KS, Uh Y et al. Genetic variations of Candida glabrata clinical isolates from Korea using multilocus sequence typing. Arch Clin Microbiol 2018; 09: [View Article]
     [Google Scholar]
  21. Amanloo S, Shams-Ghahfarokhi M, Ghahri M, Razzaghi-Abyaneh M. Genotyping of clinical isolates of Candida glabrata from Iran by multilocus sequence typing and determination of population structure and drug resistance profile. Med Mycol 2018; 56:207–215 [View Article] [PubMed]
     [Google Scholar]
  22. Biswas C, Marcelino VR, Van Hal S, Halliday C, Martinez E et al. Whole genome sequencing of Australian Candida glabrata isolates reveals genetic diversity and novel sequence types. Front Microbiol 2018; 9:2946 [View Article] [PubMed]
     [Google Scholar]
  23. Chen Y, Wu Y, Lulou K, Yao D, Ying C. Multilocus sequence typing and antifungal susceptibility of vaginal and non-vaginal Candida glabrata isolates from China. Front Microbiol 2022; 13:537 [View Article]
     [Google Scholar]
  24. Arastehfar A, Marcet-Houben M, Daneshnia F, Taj-Aldeen SJ, Batra D et al. Comparative genomic analysis of clinical Candida glabrata isolates identifies multiple polymorphic loci that can improve existing multilocus sequence typing strategy. Stud Mycol 2021; 100:100133 [View Article] [PubMed]
     [Google Scholar]
  25. Healey KR, Zhao Y, Perez WB, Lockhart SR, Sobel JD et al. Prevalent mutator genotype identified in fungal pathogen Candida glabrata promotes multi-drug resistance. Nat Commun 2016; 7:1–10 [View Article]
     [Google Scholar]
  26. Legrand M, Chan CL, Jauert PA, Kirkpatrick DT. Role of DNA mismatch repair and double-strand break repair in genome stability and antifungal drug resistance in Candida albicans. Eukaryot Cell 2007; 6:2194–2205 [View Article] [PubMed]
     [Google Scholar]
  27. Stefanini I, Stoakes E, Wu HHT, Xu-McCrae L, Hussain A et al. Genomic assembly of clinical Candida glabrata (Nakaseomyces glabrata) isolates reveals within-species structural plasticity and association with In Vitro antifungal susceptibility. Microbiol Spectr 2022; 10:e0182722 [View Article] [PubMed]
     [Google Scholar]
  28. Helmstetter N, Chybowska AD, Delaney C, Da Silva Dantas A, Gifford H et al. Population genetics and microevolution of clinical Candida glabrata reveals recombinant sequence types and hyper-variation within mitochondrial genomes, virulence genes, and drug targets. Genetics 2022; 221:iyac031 [View Article] [PubMed]
     [Google Scholar]
  29. Chapman B, Slavin M, Marriott D, Halliday C, Kidd S et al. Changing epidemiology of candidaemia in Australia. J Antimicrob Chemother 2017; 72:1103–1108 [View Article] [PubMed]
     [Google Scholar]
  30. Tan TY, Hsu LY, Alejandria MM, Chaiwarith R, Chinniah T et al. Antifungal susceptibility of invasive Candida bloodstream isolates from the Asia-Pacific region. Med Mycol 2016; 54:471–477 [View Article] [PubMed]
     [Google Scholar]
  31. Pfaller MA, Diekema DJ, Turnidge JD, Castanheira M, Jones RN. Twenty years of the SENTRY antifungal surveillance program: results for Candida species from 1997-2016. Open Forum Infect Dis 2019; 6:S79–S94 [View Article] [PubMed]
     [Google Scholar]
  32. Castanheira M, Deshpande LM, Davis AP, Carvalhaes CG, Pfaller MA. Azole resistance in Candida glabrata clinical isolates from global surveillance is associated with efflux overexpression. J Glob Antimicrob Resist 2022; 29:371–377 [View Article] [PubMed]
     [Google Scholar]
  33. Cai S, Xu J, Shao Y, Gong J, Zhao F et al. Rapid identification of the Candida glabrata species complex by high-resolution melting curve analysis. J Clin Lab Anal 2020; 34:e23226 [View Article] [PubMed]
     [Google Scholar]
  34. Gabaldón T, Gómez-Molero E, Bader O. Molecular typing of Candida glabrata. Mycopathologia 2020; 185:755–764 [View Article] [PubMed]
     [Google Scholar]
  35. Won EJ, Choi MJ, Kim M-N, Yong D, Lee WG et al. Fluconazole-resistant Candida glabrata bloodstream isolates, South Korea, 2008-2018. Emerg Infect Dis 2021; 27:779–788 [View Article] [PubMed]
     [Google Scholar]
  36. Vu BG, Stamnes MA, Li Y, Rogers PD, Moye-Rowley WS. The Candida glabrata Upc2A transcription factor is a global regulator of antifungal drug resistance pathways. PLoS Genet 2021; 17:e1009582 [View Article] [PubMed]
     [Google Scholar]
  37. Simonicova L, Moye-Rowley WS. Functional information from clinically-derived drug resistant forms of the Candida glabrata Pdr1 transcription factor. PLoS Genet 2020; 16:e1009005 [View Article] [PubMed]
     [Google Scholar]
  38. Morio F, Pagniez F, Besse M, Gay-andrieu F, Miegeville M et al. Deciphering azole resistance mechanisms with a focus on transcription factor-encoding genes TAC1, MRR1 and UPC2 in a set of fluconazole-resistant clinical isolates of Candida albicans. Int J Antimicrob Agents 2013; 42:410–415 [View Article] [PubMed]
     [Google Scholar]
  39. Sanguinetti M, Posteraro B, Fiori B, Ranno S, Torelli R et al. Mechanisms of azole resistance in clinical isolates of Candida glabrata collected during a hospital survey of antifungal resistance. Antimicrob Agents Chemother 2005; 49:668–679 [View Article] [PubMed]
     [Google Scholar]
  40. Yu SJ, Chang YL, Chen YL. Deletion of ADA2 increases antifungal drug susceptibility and virulence in Candida glabrata. Antimicrob Agents Chemother 2018; 62:e01924-17 [View Article] [PubMed]
     [Google Scholar]
  41. Rasheed M, Battu A, Kaur R. Host-pathogen interaction in Candida glabrata infection: current knowledge and implications for antifungal therapy. Expert Rev Anti Infect Ther 2020; 18:1093–1103 [View Article] [PubMed]
     [Google Scholar]
  42. Vandeputte P, Tronchin G, Larcher G, Ernoult E, Bergès T et al. A nonsense mutation in the ERG6 gene leads to reduced susceptibility to polyenes in a clinical isolate of Candida glabrata. Antimicrob Agents Chemother 2008; 52:3701–3709 [View Article] [PubMed]
     [Google Scholar]
  43. Israel S, Amit S, Israel A, Livneh A, Nir-Paz R et al. The epidemiology and susceptibility of candidemia in Jerusalem, Israel. Front Cell Infect Microbiol 2019; 9:352 [View Article] [PubMed]
     [Google Scholar]
  44. Sakita KM, Faria DR, Silva EM da, Tobaldini-Valério FK, Kioshima ES et al. Healthcare workers’ hands as a vehicle for the transmission of virulent strains of Candida spp.: a virulence factor approach. Microb Pathog 2017; 113:225–232 [View Article] [PubMed]
     [Google Scholar]
  45. Pappas PG, Lionakis MS, Arendrup MC, Ostrosky-Zeichner L, Kullberg BJ. Invasive candidiasis. Nat Rev Dis Primers 2018; 4:18026 [View Article] [PubMed]
     [Google Scholar]
  46. Colombo AL, Júnior JN de A, Guinea J. Emerging multidrug-resistant Candida species. Curr Opin Infect Dis 2017; 30:528–538 [View Article] [PubMed]
     [Google Scholar]
  47. Al-Baqsami ZF, Ahmad S, Khan Z. Antifungal drug susceptibility, molecular basis of resistance to echinocandins and molecular epidemiology of fluconazole resistance among clinical Candida glabrata isolates in Kuwait. Sci Rep 2020; 10:6238 [View Article] [PubMed]
     [Google Scholar]
  48. Pristov KE, Ghannoum MA. Resistance of Candida to azoles and echinocandins worldwide. Clin Microbiol Infect 2019; 25:792–798 [View Article] [PubMed]
     [Google Scholar]
  49. Gabaldón T, Carreté L. The birth of a deadly yeast: tracing the evolutionary emergence of virulence traits in Candida glabrata. FEMS Yeast Res 2016; 16:fov110 [View Article] [PubMed]
     [Google Scholar]
  50. Srikantha T, Lachke SA, Soll DR. Three mating type-like loci in Candida glabrata. Eukaryot Cell 2003; 2:328–340 [View Article] [PubMed]
     [Google Scholar]
  51. Robledo-Márquez K, Gutiérrez-Escobedo G, Yáñez-Carrillo P, Vidal-Aguiar Y, Briones-Martín-Del-Campo M et al. Candida glabrata encodes a longer variant of the mating type (MAT) alpha2 gene in the mating type-like MTL3 locus, which can form homodimers. FEMS Yeast Res 2016; 16:fow082 [View Article] [PubMed]
     [Google Scholar]
  52. Brockert PJ, Lachke SA, Srikantha T, Pujol C, Galask R et al. Phenotypic switching and mating type switching of Candida glabrata at sites of colonization. Infect Immun 2003; 71:7109–7118 [View Article] [PubMed]
     [Google Scholar]
  53. Boisnard S, Zhou Li Y, Arnaise S, Sequeira G, Raffoux X et al. Efficient mating-type switching in Candida glabrata induces cell death. PLoS One 2015; 10:e0140990 [View Article] [PubMed]
     [Google Scholar]
  54. Statistics Site. n.d https://www.psa.gov.qa/en/statistics1/Pages/default.aspx accessed 16 April 2023
  55. Population of Qatar by nationality; 2019 https://priyadsouza.com/population-of-qatar-by-nationality-in-2017 accessed 16 April 2023
  56. Taj-Aldeen SJ, Kolecka A, Boesten R, Alolaqi A, Almaslamani M et al. Epidemiology of candidemia in Qatar, the Middle East: performance of MALDI-TOF MS for the identification of Candida species, species distribution, outcome, and susceptibility pattern. Infection 2014; 42:393–404 [View Article]
     [Google Scholar]
  57. CLSI M60-Ed1 - Performance Standards for Antifungal Susceptibility Testing of Yeasts - 1st Edition. n.d https://webstore.ansi.org/standards/clsi/clsim60ed1 accessed 17 April 2023
  58. CLSI M59-Ed3 - Epidemiological Cutoff Values for Antifungal Susceptibility Testing - 3rd Edition. n.d https://webstore.ansi.org/standards/clsi/clsim59ed3 accessed 17 April 2023
  59. FastQC: a quality control tool for high throughput sequence data – ScienceOpen. n.d https://www.scienceopen.com/document?vid=de674375-ab83-4595-afa9-4c8aa9e4e736 accessed 18 December 2022
  60. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
     [Google Scholar]
  61. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv 2013
     [Google Scholar]
  62. Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing; 2012 https://doi.org/10.48550/arxiv.1207.3907
  63. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
     [Google Scholar]
  64. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  65. Carreté L, Ksiezopolska E, Pegueroles C, Gómez-Molero E, Saus E et al. Patterns of genomic variation in the opportunistic pathogen Candida glabrata suggest the existence of mating and a secondary association with humans. Curr Biol 2018; 28:15–27 [View Article] [PubMed]
     [Google Scholar]
  66. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 2015; 4:7 [View Article] [PubMed]
     [Google Scholar]
  67. Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res 2009; 19:1655–1664 [View Article] [PubMed]
     [Google Scholar]
  68. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  69. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:1–9 [View Article] [PubMed]
     [Google Scholar]
  70. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. Gigascience 2021; 10:giab008 [View Article] [PubMed]
     [Google Scholar]
  71. Hunter JD. Matplotlib: a 2D graphics environment. Comput Sci Eng 2007; 9:90–95 [View Article]
     [Google Scholar]
  72. Harris CR, Millman KJ, van der Walt SJ, Gommers R, Virtanen P et al. Array programming with NumPy. Nature 2020; 585:357–362 [View Article] [PubMed]
     [Google Scholar]
  73. Danecek P, Auton A, Abecasis G, Albers CA, Banks E et al. The variant call format and VCFtools. Bioinformatics 2011; 27:2156–2158 [View Article] [PubMed]
     [Google Scholar]
  74. Weig M, Jänsch L, Gross U, De Koster CG, Klis FM et al. Systematic identification in silico of covalently bound cell wall proteins and analysis of protein-polysaccharide linkages of the human pathogen Candida glabrata. Microbiology 2004; 150:3129–3144 [View Article] [PubMed]
     [Google Scholar]
  75. Priebe S, Linde J, Albrecht D, Guthke R, Brakhage AA. FungiFun: a web-based application for functional categorization of fungal genes and proteins. Fungal Genet Biol 2011; 48:353–358 [View Article] [PubMed]
     [Google Scholar]
  76. Liu X, Huang M, Fan B, Buckler ES, Zhang Z. Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 2016; 12:e1005767 [View Article] [PubMed]
     [Google Scholar]
  77. Wang J, Zhang Z. GAPIT version 3: boosting power and accuracy for genomic association and prediction. GPB 2021; 19:629–640 [View Article] [PubMed]
     [Google Scholar]
  78. Hassan Y, Chew SY, Than LTL. Candida glabrata: pathogenicity and resistance mechanisms for adaptation and survival. J Fungi 2021; 7:667 [View Article] [PubMed]
     [Google Scholar]
  79. Skrzypek MS, Binkley J, Binkley G, Miyasato SR, Simison M et al. The Candida genome database (CGD): incorporation of assembly 22, systematic identifiers and visualization of high throughput sequencing data. Nucleic Acids Res 2017; 45:D592–D596 [View Article] [PubMed]
     [Google Scholar]
  80. Bethea EK, Carver BJ, Montedonico AE, Reynolds TB. The inositol regulon controls viability in Candida glabrata. Microbiology 2010; 156:452–462 [View Article] [PubMed]
     [Google Scholar]
  81. Zhen C, Lu H, Jiang Y. Novel promising antifungal target proteins for conquering invasive fungal infections. Front Microbiol 2022; 13:911322 [View Article] [PubMed]
     [Google Scholar]
  82. Ahmed N, Mahmood MS, Ullah MA, Araf Y, Rahaman TI et al. COVID-19-associated Candidiasis: possible patho-mechanism, predisposing factors, and prevention strategies. Curr Microbiol 2022; 79:127 [View Article] [PubMed]
     [Google Scholar]
  83. Vale-Silva LA, Moeckli B, Torelli R, Posteraro B, Sanguinetti M et al. Upregulation of the adhesin gene EPA1 mediated by PDR1 in Candida glabrata leads to enhanced host colonization. mSphere 2016; 1:e00065-15 [View Article] [PubMed]
     [Google Scholar]
  84. Chowdhary A, Kathuria S, Xu J, Sharma C, Sundar G et al. Clonal expansion and emergence of environmental multiple-triazole-resistant Aspergillus fumigatus strains carrying the TR₃₄/L98H mutations in the cyp51A gene in India. PLoS One 2012; 7:e52871 [View Article] [PubMed]
     [Google Scholar]
  85. Korfanty GA, Dixon M, Jia H, Yoell H, Xu J. Genetic diversity and dispersal of Aspergillus fumigatus in arctic soils. Genes 2022; 13:19 [View Article]
     [Google Scholar]
  86. Wang Y, Xu J. Population genomic analyses reveal evidence for limited recombination in the superbug Candida auris in nature. Comput Struct Biotechnol J 2022; 20:3030–3040 [View Article] [PubMed]
     [Google Scholar]
  87. Xu J, Vilgalys R, Mitchell TG. Lack of genetic differentiation between two geographically diverse samples of Candida albicans isolated from patients infected with human immunodeficiency virus. J Bacteriol 1999; 181:1369–1373 [View Article] [PubMed]
     [Google Scholar]
  88. Wu JY, Zhou DY, Zhang Y, Mi F, Xu J. Analyses of the global multilocus genotypes of the human pathogenic yeast Candida tropicalis. Front Microbiol 2019; 10:900 [View Article] [PubMed]
     [Google Scholar]
  89. Hitchcock M, Xu J. Analyses of the global multilocus genotypes of the human pathogenic yeast Cryptococcus neoformans species complex. Genes 2022; 13:2045 [View Article] [PubMed]
     [Google Scholar]
  90. Hitchcock M, Xu J. Global analyses of multi-locus sequence typing data reveal geographic differentiation, hybridization, and recombination in the Cryptococcus gattii species complex. J Fungi 2023; 9:276 [View Article] [PubMed]
     [Google Scholar]
  91. Arastehfar A, Fang W, Pan W, Liao W, Yan L et al. Identification of nine cryptic species of Candida albicans. BMC Infect Dis 2018; 18:1–9 [View Article]
     [Google Scholar]
  92. Ene IV, Bennett RJ, Anderson MZ. Mechanisms of genome evolution in Candida albicans. Curr Opin Microbiol 2019; 52:47–54 [View Article] [PubMed]
     [Google Scholar]
  93. Matute DR, McEwen JG, Puccia R, Montes BA, San-Blas G et al. Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol Biol Evol 2006; 23:65–73 [View Article] [PubMed]
     [Google Scholar]
  94. Steenwyk JL, Rokas A, Goldman GH. Know the enemy and know yourself: addressing cryptic fungal pathogens of humans and beyond. PLoS Pathog 2023; 19:e1011704 [View Article] [PubMed]
     [Google Scholar]
  95. Samarasinghe H, You M, Jenkinson TS, Xu J, James TY. Hybridization facilitates adaptive evolution in two major fungal pathogens. Genes 2020; 11:101 [View Article] [PubMed]
     [Google Scholar]
  96. Sun S, Lin X, Coelho MA, Heitman J. Mating-system evolution: all roads lead to selfing. Curr Biol 2019; 29:R743–R746 [View Article] [PubMed]
     [Google Scholar]
  97. Salazar SB, Pinheiro MJF, Sotti-Novais D, Soares AR, Lopes MM et al. Disclosing azole resistance mechanisms in resistant Candida glabrata strains encoding wild-type or gain-of-function CgPDR1 alleles through comparative genomics and transcriptomics. G3 2022; 12:jkac110 [View Article] [PubMed]
     [Google Scholar]
  98. Khosravi Rad K, Falahati M, Roudbary M, Farahyar S, Nami S et al. Overexpression of MDR-1 and CDR-2 genes in fluconazole resistance of Candida albicans isolated from patients with vulvovaginal candidiasis. mazu-cmm 2016; 2:24–29 [View Article]
     [Google Scholar]
  99. Sanglard D, Ischer F, Monod M, Bille J. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology 1997; 143:405–416 [View Article]
     [Google Scholar]
  100. Vale-Silva L, Ischer F, Leibundgut-Landmann S, Sanglard D. Gain-of-function mutations in PDR1, a regulator of antifungal drug resistance in Candida glabrata, control adherence to host cells. Infect Immun 2013; 81:1709–1720 [View Article] [PubMed]
     [Google Scholar]
  101. Ferrari S, Ischer F, Calabrese D, Posteraro B, Sanguinetti M et al. Gain of function mutations in CgPDR1 of Candida glabrata not only mediate antifungal resistance but also enhance virulence. PLoS Pathog 2009; 5:e1000268 [View Article] [PubMed]
     [Google Scholar]
  102. Arastehfar A, Daneshnia F, Salehi M, Yaşar M, Hoşbul T et al. Low level of antifungal resistance of Candida glabrata blood isolates in Turkey: fluconazole minimum inhibitory concentration and FKS mutations can predict therapeutic failure. Mycoses 2020; 63:911–920 [View Article] [PubMed]
     [Google Scholar]
  103. Rogers PD, Vermitsky JP, Edlind TD, Hilliard GM. Proteomic analysis of experimentally induced azole resistance in Candida glabrata. J Antimicrob Chemother 2006; 58:434–438 [View Article] [PubMed]
     [Google Scholar]
  104. Fisher MC, Alastruey-Izquierdo A, Berman J, Bicanic T, Bignell EM et al. Tackling the emerging threat of antifungal resistance to human health. Nat Rev Microbiol 2022; 20:557–571 [View Article] [PubMed]
     [Google Scholar]
  105. Fan Y, Korfanty GA, Xu J. Genetic analyses of amphotericin B susceptibility in Aspergillus fumigatus. J Fungi 2021; 7:860 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001179
Loading
Population genomic analyses reveal high diversity, recombination and nosocomial transmission among Candida glabrata (Nakaseomyces glabrata) isolates causing invasive infections
M Gen 10, 001179 (2024); https://doi.org/10.1099/mgen.0.001179
/content/journal/mgen/10.1099/mgen.0.001179
/content/journal/mgen/10.1099/mgen.0.001179
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error