Candida palmioleophila: A New Emerging Threat in Brazil?
Abstract
1. Introduction
2. Materials and Methods
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Etty, T.; Heyvaert, V.; Carlarne, C.; Farber, D.; Huber, B.; van Zeben, J. Transnational Climate Law. Transnatl. Environ. Law 2018, 7, 191–200. [Google Scholar] [CrossRef]
- Garcia-Solache, M.A.; Casadevall, A. Global warming will bring new fungal diseases for mammals. mBio 2010, 18, e00061-10. [Google Scholar] [CrossRef]
- De Crecy, E.; Jaronski, S.; Lyons, B.; Lyons, T.J.; Keyhani, N.O. Directed evolution of a filamentous fungus for thermotolerance. BMC Biotechnol. 2009, 74, 74. [Google Scholar] [CrossRef]
- Casadevall, A. Don’t Forget the Fungi When Considering Global Catastrophic Biorisks. Health Secur. 2017, 15, 341–342. [Google Scholar] [CrossRef]
- Jackson, B.R.; Chow, N.; Forsberg, K.; Litvintseva, A.P.; Lockhart, S.R.; Welsh, R.; Vallabhaneni, S.; Chiller, T. On the Origins of a Species: What Might Explain the Rise of Candida auris? J. Fungi 2019, 5, 58. [Google Scholar] [CrossRef]
- Casadevall, A.; Kontoyiannis, D.P.; Robert, V. Environmental Candida auris and the Global Warming Emergence Hypothesis. mBio 2021, 12, e00360-21. [Google Scholar] [CrossRef] [PubMed]
- Pfaller, M.A.; Carvalhaes, C.G.; DeVries, S.; Rhomberg, P.R.; Castanheira, M. Impact of COVID-19 on the antifungal susceptibility profiles of isolates collected in a global surveillance program that monitors invasive fungal infections. Med. Mycol. J. 2022, 60, myac028. [Google Scholar] [CrossRef] [PubMed]
- Sugita, T.; Kagaya, K.; Takashima, M.; Suzuki, M.; Fukazawa, Y.; Nakase, T. A clinical isolate of Candida palmioleophila formerly identified as Torulopsis candida. Nippon Ishinkin Gakkai Zasshi 1999, 40, 21–25. [Google Scholar] [CrossRef]
- Stavrou, A.A.; Pérez-Hansen, A.; Lackner, M.; Lass-Flörl, C.; Boekhout, T. Elevated minimum inhibitory concentrations to antifungal drugs prevail in 14 rare species of candidemia-causing Saccharomycotina yeasts. Med. Mycol. J. 2020, 58, 987–995. [Google Scholar] [CrossRef]
- Ullmann, A.J.; Akova, M.; Herbrecht, R.; Viscoli, C.; Arendrup, M.C.; Arikan-Akdagli, S.; Bassetti, M.; Bille, J.; Calandra, T.; Castagnola, G.; et al. Fungal Infection Study Group: Guideline for the diagnosis and management of Candida diseases 2012: Adults with haematological malignancies and after haematopoietic stem cell transplantation (HCT). Clin. Microbiol. Infect. 2012, 18, 53–67. [Google Scholar] [CrossRef] [PubMed]
- Jensen, R.H.; Arendrup, M.C. Candida palmioleophila: Characterization of a previously overlooked pathogen and its unique susceptibility profile in comparison with five related species. J. Clin. Microbiol. 2011, 49, 549–556. [Google Scholar] [CrossRef] [PubMed]
- Datta, N.; Arendrup, M.C.; Saunte, J.P. First report of Candida palmioleophila endogenous endophthalmitis. Acta Ophthalmol. 2015, 93, 517–518. [Google Scholar] [CrossRef] [PubMed]
- Scapaticci, M.; Bartolini, A.; Del Chierico, F.; Accardi, C.; Di Girolamo, F.; Masotti, A.; Muraca, M.; Putignani, L. Phenotypic typing and epidemiological survey of antifungal resistance of Candida species detected in clinical samples of Italian patients in a 17 months’ period. Germs 2018, 8, 58–66. [Google Scholar] [CrossRef] [PubMed]
- Prado, T.; Fumian, T.M.; Mannarino, C.F.; Resende, P.C.; Motta, F.C.; Eppinghaus, A.L.F.; Chagas do Vale, V.H.; Soares Braz, R.M.; da Silva Ribeiro de Andrade, J.; Gonçalves Maranhão, A.; et al. Wastewater-based epidemiology as a useful tool to track SARS-CoV-2 and support public health policies at municipal level in Brazil. Water Res. 2021, 191, 116810. [Google Scholar] [CrossRef]
- Wu, F.; Xiao, A.; Zhang, J.; Moniz, K.; Endo, N.; Armas, F.; Bushman, M.; Chai, P.R.; Duvallet, C.; Erickson, T.B.; et al. Wastewater Surveillance of SARS-CoV-2 across 40 U.S. states. Water Res. 2021, 202, 117400. [Google Scholar] [CrossRef]
- Lindsley, M.D.; Hurst, S.F.; Iqbal, N.J.; Morrison, C.J. Rapid identification of dimorphic and yeast-like fungal pathogens using specific DNA probes. J. Clin. Microbiol. 2001, 39, 3505–3511. [Google Scholar] [CrossRef]
- Saitou, N.; Nei, M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4, 406–425. [Google Scholar]
- Pinto, T.N.; Kohn, A.; da Costa, G.L.; Oliveira, L.M.A.; Pinto, T.C.A.; Oliveira, M.M.E. Candida guilliermondii as an agent of postpartum subacute mastitis in Rio de Janeiro, Brazil: Case report. Front. Microbiol. 2022, 23, 964685. [Google Scholar] [CrossRef]
- Peeters, E.; Nelis, H.J.; Coenye, T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J. Microbiol. Methods 2008, 72, 157–165. [Google Scholar] [CrossRef]
- Price, M.F.; Wilkinson, I.D.; Gentry, L.O. Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia 1982, 20, 7–14. [Google Scholar] [CrossRef]
- Rüchel, R. Properties of a purified proteinase from the yeast Candida albicans. Biochim. Biophys. Acta 1981, 659, 99–113. [Google Scholar] [CrossRef]
- Aktas, E.; Yigit, N.; Ayyildiz, A. Esterase activity in various Candida species. J. Int. Med. Res. 2002, 30, 322–324. [Google Scholar] [CrossRef] [PubMed]
- Tsang, P.W. Differential phytate utilization in Candida species. Mycopathologia 2011, 172, 473–479. [Google Scholar] [CrossRef] [PubMed]
- National Committee for Clinical Laboratory Standards. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts: Approved Standard M27-A2, 2nd ed.; National Committee for Clinical Laboratory Standards: Wayne, PA, USA, 2002. [Google Scholar]
- Jarros, I.C.; Veiga, F.F.; Corrêa, J.L.; Barros, I.L.E.; Gadelha, M.C.; Voidaleski, M.F.; Pieralisi, N.; Bocchi Pedroso, R.; Vicente, V.A.; Negri, M.; et al. Microbiological and virulence aspects of Rhodotorula mucilaginosa. EXCLI J. 2020, 19, 687–704. [Google Scholar] [PubMed]
- Tsang, E.W.T.; Ingledew, W.M. Studies on the Heat Resistance of Wild Yeasts and Bacteria in Beer. J. Am. Soc. Brew. Chem. 1982, 40, 1–8. [Google Scholar] [CrossRef]
- Belbahi, A.; Bohuon, P.; Leguérinel, I.; Meot, J.-M.; Loiseau, G.; Madani, K. Heat Resistances of Candida apicola and Aspergillus niger Spores Isolated From Date Fruit Surface. J. Food Process Eng. 2015, 40, e12272. [Google Scholar] [CrossRef]
- Gonzalez, R.; Curtis, K.; Bivins, A.; Bibby, K.; Weir, M.; Yetka, K.; Thompson, H.; Keeling, D.; Mitchell, J.; Gonzalez, D. COVID-19 Surveillance in Southeastern Virginia Using Wastewater-Based Epidemiology. Water Res. 2020, 186, 01–09. [Google Scholar] [CrossRef]
- Medema, G.; Been, F.; Heijnen, L.; Petterson, S. Implementation of environmental surveillance for SARS-CoV-2 virus to support public health decisions: Opportunities and challenges. Curr. Opin. Environ. Sci. Health 2020, 17, 49–71. [Google Scholar] [CrossRef]
- Randazzo, W.; Truchado, P.; Cuevas-Ferrando, E.; Simón, P.; Allende, A.; Sánchez, G. SARS-CoV-2 RNA in wastewater anticipated COVID-19 occurrence in a low prevalence area. Water Res. 2020, 17, 49–51. [Google Scholar] [CrossRef]
- Ewbank, A.C.; Duarte-Benvenuto, A.; Zamana-Ramblas, R.; Navas-Suárez, P.E.; Gattamorta, M.A.; dos Santos-Costa, P.C.; Catão-Dias, J.L.; Sacristán, C. Case report of respiratory aspergillosis and candidiasis in wild Magellanic penguins (Spheniscus magellanicus), Brazil. Braz. J. Microbiol. 2021, 52, 967–975. [Google Scholar] [CrossRef]
- Jafari, N.; Kasra-Kermanshahi, R.; Soudi, M.R. Screening, identification and optimization of a yeast strain, Candida palmioleophila JKS4, capable of azo dye decolorization. Iran. J. Microbiol. 2013, 5, 434–440. [Google Scholar] [PubMed]
- Valderrama, B.; Ruiz, J.J.; Gutiérrez, M.S.; Alveal, K.; Caruffo, M.; Oliva, M.; Flores, H.; Silva, A.; Toro, M.; Reyes-Jara, A.; et al. Cultivable Yeast Microbiota from the Marine Fish Species Genypterus chilensis and Seriolella violacea. J. Fungi 2021, 7, 515. [Google Scholar] [CrossRef] [PubMed]
- Prasana Kummar, C.; Velmurugan, S.; Subramanian, K.; Chayiasut, C. Previously unrecorded distribution of marine sediments derived yeast isolates revealed by DNA barcoding. bioRxiv 2020. [Google Scholar] [CrossRef]
- Medeiros, A.O.; Missagia, B.S.; Brandão, L.R.; Callisto, M.; Barbosa, F.A.R.; Rosa, C.A. Water quality and diversity of yeasts from tropical lakes and rivers from the Rio Doce basin in Southeastern Brazil. Braz. J. Microbiol. 2012, 43, 1582–1594. [Google Scholar] [CrossRef]
- Enjalbert, B.; Rachini, A.; Vediyappan, G.; Pietrella, D.; Spaccapelo, R.; Vecchiarelli, A.; Brown, A.J.P.; d’Enfert, C. A multifunctional, synthetic Gaussia princeps luciferase reporter for live imaging of Candida albicans infections. Infect.Immun. 2009, 77, 4847–4858. [Google Scholar] [CrossRef]
- Brown, A.J.P.; Brown, G.D.; Netea, M.G.; Gow, N.A.R. Metabolism impacts upon Candida immunogenicity and pathogenicity at multiple levels. Trends Microbiol. 2014, 22, 614–622. [Google Scholar] [CrossRef]
- Ene, I.V.; Walker, L.A.; Schiavone, M.; Lee, K.K.; Martin-Yken, H.; Dague, E.; Gow, N.A.R.; Munro, C.A.; Brown, A.J.P. Cell Wall Remodeling Enzymes Modulate Fungal Cell Wall Elasticity and Osmotic Stress Resistance. mBio 2015, 6, e00986. [Google Scholar] [CrossRef]
- Reyna-Beltrán, E.; Iranzo, M.; Calderón-González, K.G.; Mondragón-Flores, R.; Labra-Barrios, M.L.; Mormeneo, S.; Luna-Arias, J.P. The Candida albicans ENO1 gene encodes a transglutaminase involved in growth, cell division, morphogenesis, and osmotic protection. J. Biol. Chem. 2018, 293, 4304–4323. [Google Scholar] [CrossRef]
- Casagrande Pierantoni, D.; Bernardo, M.; Mallardo, E.; Carannante, N.; Attanasio, V.; Corte, L.; Roscini, L.; Di Fiore, L.; Tascini, C.; Cardinali, G. Candida palmioleophila isolation in Italy from two cases of systemic infection, after a CHROMagar and Vitek system mis-identification as C. albicans. New Microbiol. 2020, 43, 47–50. [Google Scholar]
- Arendrup, M.C.; Bergmann, O.J.; Larsson, L.; Nielsen, H.V.; Jarløv, J.O.; Christensson, B. Detection of candidaemia in patients with and without underlying haematological disease. Clin. Microbiol. Infect. 2010, 16, 855–862. [Google Scholar] [CrossRef]
- Pincus, D.H.; Orenga, S.; Chatellier, S. Yeast identification—Past, present and future methods. Med. Mycol. 2007, 45, 97–121. [Google Scholar] [CrossRef]
- Santos, C.; Lima, N.; Sampaio, P.; Pais, C. Matrix-assisted laser desorption/ionization time-of-flight intact cell mass spectrometry (MALDI-TOF-ICMS) to detect emerging pathogenic Candida species. Diagn. Microb. Infect. Dis. 2011, 71, 304–308. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, M.M.E.; Santos, C.; Sampaio, P.; Romeo, O.; Almeida-Paes, R.; Pais, C.; Zancopé-Oliveira, R.M. Development and optimization of a new MALDI-TOF protocol for identification of the Sporothrix species complex. Res. Microbiol. 2015, 166, 102–110. [Google Scholar] [CrossRef] [PubMed]
- Valero, C.; Buitrago, M.J.; Gago, S.; Quiles-Melero, I.; García-Rodríguez, J. A matrix-assisted laser desorption/ionization time of flight mass spectrometry reference database for the identification of Histoplasma capsulatum. Med. Mycol. J. 2017, 56, 307–314. [Google Scholar] [CrossRef] [PubMed]
- Harriott, M.M.; Lilly, E.A.; Rodriguez, T.E.; Fidel, P.L.; Noverr, M.C. Candida albicans forms biofilms on the vaginal mucosa. Microbiology 2010, 156, 3635–3644. [Google Scholar] [CrossRef]
- Sanguinetti, M.; Posteraro, B.; Lass-Flörl, C. Antifungal drug resistance among Candida species: Mechanisms and clinical impact. Mycoses 2015, 58, 2–13. [Google Scholar] [CrossRef] [PubMed]
- Pristov, K.E.; Ghannoum, M.A.; FIDSA. Resistance of Candida to azoles and echinocandins worldwide. Clin. Microbiol. Infect. 2019, 25, 792–798. [Google Scholar] [CrossRef] [PubMed]
- Pfaller, M.A.; Diekema, D.J. Epidemiology of Invasive Candidiasis: A Persistent Public Health Problem. Clin. Microbiol. Rev. 2007, 20, 133–163. [Google Scholar] [CrossRef] [PubMed]
- Mroczyńska, M.; Brillowska-Dąbrowska, A. Virulence of Clinical Candida Isolates. Pathogens 2021, 10, 466. [Google Scholar] [CrossRef]
- De Souza, P.C.; Morey, A.T.; Castanheira, G.M.; Bocate, K.P.; Panagio, L.A.; Ito, F.A.; Furlaneto, M.C.; Yamada-Ogatta, S.F.; Costa, I.N.; Mora-Montes, H.M.; et al. Tenebrio molitor (Coleoptera: Tenebrionidae) as an alternative host to study fungal infections. J. Microbiol. Methods 2015, 118, 182–186. [Google Scholar] [CrossRef]
Sample | Biochemical Identification | Probability Identification | Chromoagar Candida 37 °C | Chromoagar Candida Plus 37 °C | MALDI-TOF MS | ITS (Parcial Sequencing) | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
(VITEK 2 System) | VITEK2 (%) | LT | LPWH | LGWH | LTPH | TQ | WMWH | LBWH | LB | TPH | LTWH | |||
ESG03 | C. albicans/C. famata/C. parapsilosis | 33 | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | C. palmioleophila | C. palmioleophila |
ESG13 | C. tropicalis/C. parapsilosis | 50 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 0 | C. palmioleophila | C. palmioleophila |
ESG15 | C. famata | 92 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 0 | 0 | C. palmioleophila | C. palmioleophila |
ESG17 | C. parapsilosis | 91 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | C. palmioleophila | C. palmioleophila |
ESG04 | Kodamaea ohmeri | 94 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 0 | 0 | C. palmioleophila | C. palmioleophila |
ESG20 | C. famata | 88 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | C. palmioleophila | C. palmioleophila |
ESG07 | C. parapsilosis | 88 | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | C. palmioleophila | C. palmioleophila |
Samples | Amphotericin B | Fluconazole | Voriconazole | Caspofungin | Micafungin | Flucytosine | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
µg/mL (Cut-Off) | µg/mL (Cut-Off) | µg/mL (Cut-Off) | µg/mL (Cut-Off) | µg/mL (Cut-Off) | µg/mL (Cut-Off) | |||||||
Vitek2 | CLSI | Vitek2 | CLSI | Vitek2 | CLSI | Vitek2 | CLSI | Vitek2 | CLSI | Vitek2 | CLSI | |
ESG 03 | 1 (S) | 0.25 (S) | 8 (R) | 4 (S) | £ 0.12 (S) | *** | 0.25 (S) | *** | £ 0.06 (S) | *** | £ 1 (S) | *** |
ESG 04 | *** | 0.5 (S) | *** | 16 (SDD) | *** | *** | *** | *** | *** | *** | *** | *** |
ESG 07 | 1 (S) | 0.25 (S) | 2 (S) | 16 (SDD) | £ 0.12 (S) | *** | 0.25 (S) | *** | £ 0.06 (S) | *** | £ 1 (S) | *** |
ESG 13 | 0.5 (S) | 0.25 (S) | 1 (S) | 1 (S) | £ 0.12 (S) | *** | £ 0.12 (S) | *** | £ 0.06 (S) | *** | £ 1 (S) | *** |
ESG 15 | *** | 0.25 (S) | *** | 64 (R) | *** | *** | *** | *** | *** | *** | *** | *** |
ESG 17 | 1 (S) | 0.5 (S) | 8 (R) | 32 (SDD) | *** | *** | £ 0.12 (S) | *** | 0.25 (S) | *** | £ 0.06 (S) | *** |
ESG 20 | *** | 0.25 (S) | *** | 16 (SDD) | *** | *** | £ 0.12 (S) | *** | 0.25 (S) | *** | £ 0.06 (S) | *** |
MIC50 | 1 | 0.25 | 2 | 16 | £ 0.12 | *** | 0.25 | *** | £ 0.06 | *** | £ 1 | *** |
MIC90 | 1 | 0.5 | 8 | 32 | £ 0.12 | *** | 0.25 | *** | £ 0.06 | *** | £ 1 | *** |
MIC Range | 0.5–1 | 0.25–0.5 | 44774 | 23377 | £ 0.12 | *** | £ 0.12–0.25 | *** | £ 0.06 | *** | £ 1 | *** |
Samples | Biofim | Esterase | Aspartic Protease | Phytase | Phospholipase |
---|---|---|---|---|---|
ESG 03 | 0.448 ± 0.092 | 0.63 ± 0.02 | 1.00 ± 0.00 | 1.00 ± 0.00 | 1.00 ± 0.00 |
ESG 04 | 1.008 ± 0.156 | 1.00 ± 0.00 | 0.52 ± 0.09 | 0.67 ± 0.07 | 1.00 ± 0.00 |
ESG 07 | 0.449 ± 0.096 | 0.62 ± 0.01 | 1.00 ± 0.00 | 1.00 ± 0.00 | 1.00 ± 0.00 |
ESG 13 | 0.811 ± 0.133 | 0.64 ± 0.01 | 0.56 ± 0.02 | 0.59 ± 0.04 | 1.00 ± 0.00 |
ESG 15 | 0.409 ± 0.096 | 0.56 ± 0.01 | 1.00 ± 0.00 | 1.00 ± 0.00 | 1.00 ± 0.00 |
ESG 17 | 0.239 ± 0.051 | 0.55 ± 0.01 | 1.00 ± 0.00 | 1.00 ± 0.00 | 1.00 ± 0.00 |
ESG 20 | 0.248 ± 0.065 | 0.61 ± 0.01 | 1.00 ± 0.00 | 1.00 ± 0.00 | 1.00 ± 0.00 |
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Costa, G.L.d.; Negri, M.; Miranda, R.P.R.d.; Corrêa-Moreira, D.; Pinto, T.C.A.; Ramos, L.d.S.; Ferreira, D.G.; Salomão, B.; Fumian, T.M.; Mannarino, C.F.; et al. Candida palmioleophila: A New Emerging Threat in Brazil? J. Fungi 2023, 9, 770. https://doi.org/10.3390/jof9070770
Costa GLd, Negri M, Miranda RPRd, Corrêa-Moreira D, Pinto TCA, Ramos LdS, Ferreira DG, Salomão B, Fumian TM, Mannarino CF, et al. Candida palmioleophila: A New Emerging Threat in Brazil? Journal of Fungi. 2023; 9(7):770. https://doi.org/10.3390/jof9070770
Chicago/Turabian StyleCosta, Gisela Lara da, Melyssa Negri, Rodrigo Prado Rodrigues de Miranda, Danielly Corrêa-Moreira, Tatiana Castro Abreu Pinto, Livia de Souza Ramos, Deisiany Gomes Ferreira, Bruna Salomão, Tulio Machado Fumian, Camille Ferreira Mannarino, and et al. 2023. "Candida palmioleophila: A New Emerging Threat in Brazil?" Journal of Fungi 9, no. 7: 770. https://doi.org/10.3390/jof9070770
APA StyleCosta, G. L. d., Negri, M., Miranda, R. P. R. d., Corrêa-Moreira, D., Pinto, T. C. A., Ramos, L. d. S., Ferreira, D. G., Salomão, B., Fumian, T. M., Mannarino, C. F., Prado, T., Miagostovich, M. P., Santos, A. L. S. d., & Oliveira, M. M. E. (2023). Candida palmioleophila: A New Emerging Threat in Brazil? Journal of Fungi, 9(7), 770. https://doi.org/10.3390/jof9070770