Abstract
The human oral cavity is normally colonized by microorganisms including bacteria, fungi, archaea, viruses and protozoa. The aim of this study was to determine the frequency of Candida spp., in de oral cavity in a group of medical students from the north of Mexico. Oral sample were obtained from 240 healthy students. The specimens were analyzed by traditional microbiology cultures and DNA sequencing. Candida spp., grew in Sabouraud dextrose agar from 57 samples and subsequently were isolated and phenotyped. The definitive identification to the species level was done by sequence analysis. The yeasts were identified as follow: 28 Clavispora lusitaniae, 20 Candida albicans, 5 Pichia kudriavzevii and 4 Candida parapsilosis. Our findings revealed that 23.75% of the healthy population has a potential pathogen in their mouth. Surprisingly, C. albicans is not the predominant yeast; instead other non-Candida species are the colonizers of the oral cavity as normal microbiota. C. lusitaniae is considered an emerging opportunistic pathogen in immunosuppressive patients. This paper pretends to highlight the presence of this yeast in the oral cavity in immunocompetent young adults.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Montelongo-Jauregui D, Lopez-Ribot JL (2018) Candida interactions with the oral bacterial microbiota. J Fungi. https://doi.org/10.3390/jof4040122
Baker JL, Bor B, Agnello M, Shi W, He X (2017) Ecology of the oral microbiome: beyond bacteria. Trends Microbiol. https://doi.org/10.1016/j.tim.2016.12.012
Bandara HMHN, Panduwawala CP, Samaranayake LP (2019) Biodiversity of the human oral mycobiome in health and disease. Oral Dis. https://doi.org/10.1111/odi.12899
Ghannoum MA et al (2010) Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000713
Wu J et al (2014) Prevalent drug resistance among oral yeasts from asymptomatic patients in Hainan, China. Mycopathologia 177:299–307. https://doi.org/10.1007/s11046-014-9747-3
Romo JA, Kumamoto CA (2020) On commensalism of candida. J Fungi 6:16. https://doi.org/10.3390/jof6010016
Di Cosola M, Cazzolla AP, Charitos IA, Ballini A, Inchingolo F, Santacroce L (2021) Candida albicans and oral carcinogenesis. A brief review. J Fungi 7:476. https://doi.org/10.3390/jof7060476
Kondori N et al (2021) Candida species as commensal gut colonizers: a study of 133 longitudinally followed Swedish infants. Med Mycol 58:485–492. https://doi.org/10.1093/MMY/MYZ091
Butler G et al (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657–662. https://doi.org/10.1038/nature08064
Priest SJ, Lorenz MC (2015) Characterization of virulence-related phenotypes in Candida species of the CUG clade. Eukaryot Cell 14:931–940. https://doi.org/10.1128/EC.00062-15
Merseguel KB et al (2015) Genetic diversity of medically important and emerging Candida species causing invasive infection. BMC Infect Dis 15:57. https://doi.org/10.1186/s12879-015-0793-3
Pérez-Brito D et al (2015) Genetic diversity of Clavispora lusitaniae isolated from Agave fourcroydes Lem, as revealed by DNA fingerprinting. J Microbiol 53:14–20. https://doi.org/10.1007/s12275-015-4373-4
Rodrigues de Miranda L (1979) Clavispora, a new yeast genus of the Saccharomycetales. Antonie Van Leeuwenhoek 45:479–483. https://doi.org/10.1007/BF00443285
Kraepelin G (1984) J. A. Barnett, R. W. Payne and D. Yarrow, Yeasts: Characteristics and Identification. 811 S., 488 (Mikrophotos) Abb., zahlreiche Tabellen. Cambridge 1983. Cambridge University Press. £75.00. Z Allg Mikrobiol 24:436. https://doi.org/10.1002/jobm.19840240703
Merz WG (1990) Candida albicans strain delineation. Clin Microbiol Rev 3:321–334. https://doi.org/10.1128/CMR.3.4.321
Gouba N, Raoult D, Drancourt M (2014) Eukaryote culturomics of the gut reveals new species. PLoS ONE 9:e106994. https://doi.org/10.1371/journal.pone.0106994
Horváth M et al (2021) Oral epithelial cells distinguish between candida species with high or low pathogenic potential through microRNA regulation. mSystems 6:e00163-e221. https://doi.org/10.1128/msystems.00163-21
Chan GF, Gan HM, Ling HL, Rashid NAA (2012) Genome sequence of Pichia kudriavzevii M12, a potential producer of bioethanol and phytase. Eukaryot Cell 11:1300–1301. https://doi.org/10.1128/EC.00229-12
Madeeha IR, Ikram A, Imran M (2016) A preliminary insight of correlation between human fecal microbial diversity and blood lipid profile. Int J Food Sci Nutr 67:1–7. https://doi.org/10.1080/09637486.2016.1201791
Nagarathnamma T et al (2017) Outbreak of Pichia kudriavzevii fungaemia in a neonatal intensive care unit. J Med Microbiol 66:1759–1764. https://doi.org/10.1099/jmm.0.000645
Hassani Abharian P, Dehghan P, Hassani-Abharian P, Jabalameli Z (2020) Frequency of Candida species in the oral cavity of narcotics and stimulants smokers in Isfahan, using polymerase chain reaction-restriction fragment length polymorphism method. Adv Biomed Res 9:30. https://doi.org/10.4103/abr.abr_38_20
Odds FC, Bernaerts R (1994) CHROMagar Candida, a new differential isolation medium for presumptive identification of clinically important Candida species. J Clin Microbiol. https://doi.org/10.1128/jcm.32.8.1923-1929.1994
Richini-Pereira VB, de Camargo RMP, Bagagli E, Marques SA (2012) White piedra: molecular identification of Trichosporon inkin in members of the same family. Rev Soc Bras Med Trop 45:402–404. https://doi.org/10.1590/s0037-86822012000300025
Montoya AM, Luna-Rodríguez CE, Gracia-Robles G, Rojas OC, González GM (2019) In vitro lytic activity and antifungal susceptibility of infrequently isolated yeasts. Arch Microbiol 201:1147–1149. https://doi.org/10.1007/s00203-019-01684-2
Chenna R et al (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500. https://doi.org/10.1093/nar/gkg500
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. https://doi.org/10.1093/molbev/mst197
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Pinto-Almazán R et al (2022) Frequency of Candida spp. in the oral cavity of asymptomatic preschool Mexican children and its association with nutritional status. Children 9:1510. https://doi.org/10.3390/children9101510
Calderone RA, Fonzi WA (2001) Virulence factors of Candida albicans. Trends Microbiol 9:327–335. https://doi.org/10.1016/S0966-842X(01)02094-7
Mun MSS, Yap T, Alnuaimi AD, Adams GG, Mccullough MJ (2016) Oral candidal carriage in asymptomatic patients. Aust Dent J 61:190–195. https://doi.org/10.1111/adj.12335
Monteiro-Da-Silva F, Araujo R, Sampaio-Maia B (2014) Interindividual variability and intraindividual stability of oral fungal microbiota over time. Med Mycol 52:498–505. https://doi.org/10.1093/mmy/myu027
Takuma A et al (2023) Failure of liposomal amphotericin B therapy in patients with severe pancreatitis complicated by Candida lusitaniae infection. J Infect Chemother 29:208–211. https://doi.org/10.1016/j.jiac.2022.10.011
Giovanoulis V et al (2022) Prosthetic knee joint infection due to Candida lusitaniae: a diagnostic and therapeutic odyssey: a case study. Diagnostics 12:2640. https://doi.org/10.3390/diagnostics12112640
Yoneda T, Hoshina T, Fukuda T, Ohama N, Murakawa S, Kusuhara K (2023) A previously unreported case of suppurative thrombophlebitis due to Clavispora lusitaniae. J Med Mycol 33:101390. https://doi.org/10.1016/j.mycmed.2023.101390
Mendoza-Reyes DF, Gómez-Gaviria M, Mora-Montes HM (2022) Candida lusitaniae: biology, pathogenicity, virulence factors, diagnosis, and treatment. Infect Drug Resist 15:5121–5135. https://doi.org/10.2147/IDR.S383785
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All authors contributed to the study conception and design. Samples recovery, microbial culture, by DC-A. DNA extraction and data collection were performed by OCR, CA-M, SM-O and AMM. DNA sequence analysis and the first draft of the manuscript was written by OCR and RG-Á. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Rojas, O.C., Amaral-Montesino, C., Mendoza-Olazaran, S. et al. Isolation of Clavispora lusitaniae from the Oral Cavity of Immunocompetent Young Adults from the North of Mexico. Indian J Microbiol (2023). https://doi.org/10.1007/s12088-023-01145-x
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DOI: https://doi.org/10.1007/s12088-023-01145-x