Clonal evolution of Candida albicans, Candida glabrata and Candida dubliniensis at oral niche level in health and disease

References

• Zaura E, Keijser BJF, Huse SM, et al. Defining the healthy “core microbiome“ of oral microbial communities. BMC Microbiol. 2009;9(1):259.
   PubMedGoogle Scholar
• Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R, et al. The oral metagenome in health and disease. Isme J. 2011;1–12. https://doi.org/10.1038/ismej.2011.85.
   Google Scholar
• Wright CJ, Burns LH, Jack AA, et al. Microbial interactions in building of communities. Mol Oral Microbiol. 2013;28(2):83–101.
   PubMed Web of Science ®Google Scholar
• Falsetta ML, Klein MI, Colonne PM, et al. Symbiotic Relationship between Streptococcus mutans and Candida albicans Synergizes Virulence of Plaque Biofilms In Vivo. Infect Immun. 2014;82(5):1968–1981.
   PubMed Web of Science ®Google Scholar
• Metwalli KH, Khan SA, Krom BP, et al. Streptococcus mutans, Candida albicans, and the Human Mouth: a Sticky Situation. Heitman J, editor PLoS Pathog. 2013;910:e1003616.
   PubMed Web of Science ®Google Scholar
• McManus BA, Maguire R, Cashin PJ, et al. Enrichment of multilocus sequence typing clade 1 with oral Candida albicans isolates in patients with untreated periodontitis. J Clin Microbiol. 2012;50(10):3335–3344.
   Web of Science ®Google Scholar
• Canabarro A, Valle C, Farias MR, et al. Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res. 2013;48(4):428–432.
   Web of Science ®Google Scholar
• Odds FC, Jacobsen MD. Multilocus sequence typing of pathogenic Candida species. Eukaryot Cell. 2008;7(7):1075–1084.
   Google Scholar
• McManus BA, Coleman DC, Moran G, et al. Multilocus sequence typing reveals that the population structure of Candida dubliniensis is significantly less divergent than that of Candida albicans. J Clin Microbiol. 2008;46(2):652–664.
   Web of Science ®Google Scholar
• Dodgson AR, Pujol C, Denning DW, Dodgson AR, Pujol C, Denning DW, Soll DR, Fox AJ. Multilocus sequence typing of Candida glabrata reveals geographically enriched clades. J Clin Microbiol. 2003;41(12):5709–5717..
   Web of Science ®Google Scholar
• Tavanti A, Davidson AD, Johnson EM, et al. Multilocus sequence typing for differentiation of strains of Candida tropicalis. J Clin Microbiol. 2005;43(11):5593–5600.
   Web of Science ®Google Scholar
• Bougnoux M-E, Tavanti A, Bouchier C, et al. Collaborative consensus for optimized multilocus sequence typing of Candida albicans. J Clin Microbiol. 2003;41(11):5265–5266.
   Web of Science ®Google Scholar
• Jacobsen MD, Gow NAR, Mcj M, et al. Strain typing and determination of population structure of Candida krusei by multilocus sequence typing. J Clin Microbiol. 2007;45:317–323.
   Web of Science ®Google Scholar
• Pujol C, Joly S, Lockhart SR, et al. Parity among the randomly amplified polymorphic DNA method, multilocus enzyme electrophoresis, and Southern blot hybridization with the moderately repetitive DNA probe Ca3 for fingerprinting Candida albicans.. J Clin Microbiol. 1997;35(9):2348–2358.
   Web of Science ®Google Scholar
• Gow NAR. A developmental program for Candida commensalism. Nat Genet. 2013;45(9):967–968.
   Web of Science ®Google Scholar
• Pande K, Chen C, Noble SM. Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat Genet. 2013;45(9):1088–1091.
   PubMed Web of Science ®Google Scholar
• Miller MG, Johnson AD. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell. 2002;110(3):293–302.
   PubMed Web of Science ®Google Scholar
• Hickman MA, Zeng G, Forche A, et al. The ‘obligate diploid’ Candida albicans forms mating-competent haploids. Nature. 2013;494(7435):55–59.
   PubMed Web of Science ®Google Scholar
• Rosenberg SM. Stress-Induced Loss of Heterozygosity in Candida: a Possible Missing Link in the Ability to Evolve. Commentary. 2011;2:3–6.
   Google Scholar
• Jeffares DC, Rallis C, Rieux A, et al. The genomic and phenotypic diversity of Schizosaccharomyces pombe. Nat Genet. 2015;47(3):235–241.
   Web of Science ®Google Scholar
• Abdolrasouli A, Rhodes J, Beale MA, et al. Genomic Context of Azole Resistance Mutations in Aspergillus fumigatus Determined Using Whole-Genome Sequencing. MBio. 2015;6:1–11.
   Web of Science ®Google Scholar
• Laverdière M, Lalonde RG, Baril J-G, et al. Progressive loss of echinocandin activity following prolonged use for treatment of Candida albicans oesophagitis. J Antimicrob Chemother. 2006;57(4):705–708.
   PubMed Web of Science ®Google Scholar
• McManus BA, McGovern E, Moran GP, et al. Microbiological Screening of Irish Patients with Autoimmune Polyendocrinopathy-Candidiasis-Ectodermal Dystrophy Reveals Persistence of Candida albicans Strains, Gradual Reduction in Susceptibility to Azoles, and Incidences of Clinical Signs of Oral Candidiasis without Culture Evidence. J Clin Microbiol. 2011;49(5):1879–1889.
   PubMed Web of Science ®Google Scholar
• Lott TJ, Frade JP, Lockhart SR. Multilocus sequence type analysis reveals both clonality and recombination in populations of Candida glabrata bloodstream isolates from U.S. surveillance studies. Eukaryot Cell. 2010;9(4):619–625.
   Google Scholar
• Wu Y, Zhou H, Wang J, et al. Analysis of the clonality of Candida tropicalis strains from a general hospital in Beijing using multilocus sequence typing. PLoS One. 2012;7(11):e47767.
   Web of Science ®Google Scholar
• Gee SF, Joly S, Soll DR, et al. Identification of four distinct genotypes of Candida dubliniensis and detection of microevolution in vitro and in vivo. J Clin Microbiol. 2002;40(2):556–574.
   Web of Science ®Google Scholar
• Magri MMC, Gomes-Gouvêa MS, De freitas VLT, et al. Multilocus Sequence Typing of Candida tropicalis Shows the Presence of Different Clonal Clusters and Fluconazole Susceptibility Profiles in Sequential Isolates from Candidemia Patients in São Paulo, Brazil. J Clin Microbiol. 2013;51(1):268–277.
   Web of Science ®Google Scholar
• Shin JH, Chae MJ, Song JW, et al. Changes in karyotype and azole susceptibility of sequential bloodstream isolates from patients with Candida glabrata candidemia. J Clin Microbiol. 2007;45(8):2385–2391.
   Web of Science ®Google Scholar
• Siikala E, Rautemaa R, Richardson M, et al. Persistent Candida albicans colonization and molecular mechanisms of azole resistance in autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) patients. J Antimicrob Chemother. 2010;65(12):2505–2513.
   PubMed Web of Science ®Google Scholar
• Coco BJ, Bagg J, Cross LJ, et al. Mixed Candida albicans and Candida glabrata populations associated with the pathogenesis of denture stomatitis. Oral Microbiol Immunol. 2008;23(5):377–383.
   PubMedGoogle Scholar
• Coleman D, Sullivan D, Harrington B, et al. Molecular and phenotypic analysis of Candida dubliniensis: a recently identified species linked with oral candidosis in HIV-infected and AIDS patients. Oral Dis. 1997;3(S1):S96–101.
   PubMedGoogle Scholar
• Abdulrahim MH, McManus BA, Flint SR, et al. Genotyping Candida albicans from Candida Leukoplakia and Non-Candida Leukoplakia Shows No Enrichment of Multilocus Sequence Typing Clades but Enrichment of ABC Genotype C in Candida Leukoplakia. PLoS One. 2013;8(9):e73738.
   Web of Science ®Google Scholar
• Yang XQ, Zhang Q, Lu LY, et al. Genotypic distribution of Candida albicans in dental biofilm of Chinese children associated with severe early childhood caries. Arch Oral Biol. 2012;57(8):1048–1053.
   PubMed Web of Science ®Google Scholar
• Cohen L. Oral candidiasis – it’s diagnosis and treatment. . Journal of Oral medicine. 1972;27(1):7–11.
   Google Scholar
• British Society of Periodontitis. British Society of periodontitis. In: British Society of periodontitis. 2015
   Google Scholar
• Cooke VM, Miles RJ, Price RG, et al. New Chromogenic Agar Medium for the Identification of Candida spp. Appl Environ Microbiol. 2002;68(7):3622–3627.
   Web of Science ®Google Scholar
• Liguori G, Lucariello A, Colella G, et al. Rapid identification of Candida species in oral rinse solutions by PCR. J Clin Pathol. 2006;60(9):1035–1039.
   Web of Science ®Google Scholar
• CLSI. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard. CLSI document M27-A3 3rd. Clinical and Laboratory Standards Institute; 2008.
   Google Scholar
• Rodriguez-Tudela JL, Arendrup MC, Barchiesi F. EUCAST definitive document EDef 7.1: method for the determination of broth dilution MICs of antifungal agents for fermentative yeasts. Clin Microbiol Infect. 2008;14(4):398–405.
   Web of Science ®Google Scholar
• Tavanti A, Gow NAR, Senesi S, et al. Optimization and validation of multilocus sequence typing for Candida albicans. J Clin Microbiol. 2003;41(8):3765–3776.
   Web of Science ®Google Scholar
• Jacobsen MD, Rattray AMJ, Gow NAR, et al. Mitochondrial haplotypes and recombination in Candida albicans. Med Mycol. 2008;46:647–654.
   PubMed Web of Science ®Google Scholar
• Crooks GE. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188–1190.
   PubMed Web of Science ®Google Scholar
• Sievers F, Wilm A, Dineen D, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega.. Mol Syst Biol. 2011;7:7.
   Web of Science ®Google Scholar
• Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23(2):254–267.
   PubMed Web of Science ®Google Scholar
• Francisco AP, Bugalho M, Ramirez M, et al. Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinformatics. 2009;10(1):1–15.
   Google Scholar
• Drummond AJ, Rambaut RA. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7(1):1–8.
   PubMedGoogle Scholar
• Drummond AJ, Suchard MA, Xie D, et al. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution. 2012;29(8):1969–1973.
   PubMed Web of Science ®Google Scholar
• Rambaut A. FigTree Version 1.4.0. 2006. Available: http://tree.bio.ed.ac.uk/software/figtree/
   Google Scholar
• Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 2001;68(4):978–989.
   PubMed Web of Science ®Google Scholar
• Gow NAR, van de Veerdonk FL, Brown AJP, et al. Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol. 2012;10(2):112–122.
   Web of Science ®Google Scholar
• Spampinato C, Leonardi D. Molecular Fingerprints to Identify Candida Species. Biomed Res Int. 2013;2013:923742.
   Web of Science ®Google Scholar
• Ford CB, Funt JM, Abbey D, et al. The evolution of drug resistance in clinical isolates of candida albicans. Elife. 2015;2015:1–27.
   Google Scholar
• Takakura S, Ichiyama S, Bain JM, et al. Comparison of Candida albicans strain types among isolates from three countries. Int J Med Microbiol. 2008;298(7–8):663–668.
   Web of Science ®Google Scholar
• Shin JH, Bougnoux M-E, D’Enfert C, et al. Genetic diversity among Korean Candida albicans bloodstream isolates: assessment by multilocus sequence typing and restriction endonuclease analysis of genomic DNA by use of BssHII. J Clin Microbiol. 2011;49(7):2572–2577.
   Web of Science ®Google Scholar
• Cross L, Williams D, Sweeney C, et al. Evaluation of the recurrence of denture stomatitis and Candida colonization in a small group of patients who received itraconazole. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology & Endodontics. 2004;97(3):351–358.
   Web of Science ®Google Scholar
• Yigit N, Aktas E, Dagistan S, et al. Investigating Biofilm Production, Coagulase and Hemolytic Activity in Candida Species Isolated From Denture Stomatitis Patients. The Eurasian Journal of Medicine. 2011;43(1):27–32.
   Google Scholar
• Qi QG, Hu T, Zhou XD. Frequency, species and molecular characterization of oral Candida in hosts of different age in China. J Oral Pathol Med. 2005;34(6):352–356.
   Web of Science ®Google Scholar
• Jabra-Rizk MA, Ferreira SM, Sabet M, et al. Recovery of Candida dubliniensis and other yeasts from human immunodeficiency virus-associated periodontal lesions. J Clin Microbiol. 2001;39(12):4520–4522.
   Web of Science ®Google Scholar
• Sardi JCO, Duque C, Camargo GACG. Periodontal conditions and prevalence of putative periodontopathogens and Candida spp. in insulin-dependent type 2 diabetic and non-diabetic patients with chronic periodontitis—A pilot study. Arch Oral Biol. 2011;56(10):1098–1105.
   Web of Science ®Google Scholar
• Urzúa B, Hermosilla G, Gamonal J, et al. Yeast diversity in the oral microbiota of subjects with periodontitis: candida albicans and Candida dubliniensis colonize the periodontal pockets. Med Mycol. 2008;46(8):783–793.
   PubMed Web of Science ®Google Scholar
• Keten D, Keten HS, Goktas MT, et al. Oral Candida carriage and prevalence of Candida species among Maras powder users and non-users.. J Oral Pathol Med. 2015;44(7):502–506.
   Web of Science ®Google Scholar
• Deorukhkar SC, Saini S, Mathew S. Non-albicans Candida Infection: an Emerging Threat. Interdisciplinary Perspectives on Infectious Diseases. 2014;2014:1–7.
   Google Scholar
• Ropars J, Maufrais C, Diogo D, et al. Gene flow contributes to diversification of the major fungal pathogen Candida albicans.. Nat Commun. 2018;9(1):9.
   Google Scholar
• Forche A, Magee PT, Selmecki A, et al. Evolution in Candida albicans Populations During a Single Passage Through a Mouse Host. Genetics. 2009;182(3):799–811.
   Web of Science ®Google Scholar
• Dodgson AR, Pujol C, Pfaller MA, Dodgson AR, Pujol C, Pfaller MA, Denning DW, Soll DR. Evidence for recombination in Candida glabrata. Fungal Genet Biol. 2005;42(3):233–243..
   Web of Science ®Google Scholar
• Enache-Angoulvant A, Bourget M, Brisse S, et al. Multilocus microsatellite markers for molecular typing of Candida glabrata: application to analysis of genetic relationships between bloodstream and digestive system isolates. J Clin Microbiol. 2010;48(11):4028–4034.
   Web of Science ®Google Scholar
• Carreté L, Ksiezopolska E, Gómez-Molero E, et al. Genome comparisons of Candida glabrata serial clinical isolates reveal patterns of genetic variation in infecting clonal populations. Front Microbiol. 2019;10:1–13.
   Web of Science ®Google Scholar
• McManus BA, Sullivan DJ, Moran GP, et al. Genetic Differences between Avian and Human Isolates of Candida dubliniensis. Emerg Infect Dis. 2009;15(9):1467–1470.
   Web of Science ®Google Scholar
• Gómez-Molero E, Willis JR, Dudakova A, et al. Phenotypic Variability in a Coinfection With Three Independent Candida parapsilosis Lineages. Front Microbiol. 2020;11:1–10.
   Web of Science ®Google Scholar
• Hijazi K, Morrison RW, Mukhopadhya I, et al. Oral bacterial diversity is inversely correlated with mucosal inflammation. Oral Dis. 2020;26(7):1566–1575.
   PubMed Web of Science ®Google Scholar
• Boers SA, van der Reijden WA, Jansen R. High-throughput multilocus sequence typing: bringing molecular typing to the next level. PLoS One. 2012;7(7):e39630.
   PubMed Web of Science ®Google Scholar
• Singh P, Foley SL, Nayak R, et al. Massively parallel sequencing of enriched target amplicons for high-resolution genotyping of Salmonella serovars. Mol Cell Probes. 2013;27(2):80–85.
   Web of Science ®Google Scholar
• Nübel U, Dordel J, Kurt K, et al. A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus. PLoS Pathog. 2010;6(4):e1000855.
   Web of Science ®Google Scholar
• Wilson DJ, Chitnis CE. Insights from genomics into bacterial pathogen populations. PLoS Pathog. 2012;8(9):e1002874.
   Web of Science ®Google Scholar
• Ellison CE, Hall C, Kowbel D, et al. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci. 2011;108(7):2831–2836.
   Web of Science ®Google Scholar
• Cornejo OE, Lefébure T, Bitar PDP, et al. Evolutionary and population genomics of the cavity causing bacteria Streptococcus mutans. Mol Biol Evol. 2013;30(4):881–893.
   PubMed Web of Science ®Google Scholar
• Beale MA, Sabiiti W, Robertson EJ, et al. Genotypic Diversity Is Associated with Clinical Outcome and Phenotype in Cryptococcal Meningitis across Southern Africa. PLoS Negl Trop Dis. 2015;9(6):e0003847.
   Web of Science ®Google Scholar
• Carreté L, Ksiezopolska E, Pegueroles C, 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(1):15–27.e7.
   Web of Science ®Google Scholar
• Segata N, Waldron L, Ballarini A, et al. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods. 2012;9(8):811–814.
   PubMed Web of Science ®Google Scholar
• Tu Q, He Z, Zhou J. Strain/species identification in metagenomes using genome-specific markers. Nucleic Acids Res. 2014;42(8):1–12.
   Web of Science ®Google Scholar