Characterization of three native Streptomyces isolates that inhibit the growth of fluconazole-resistant Candida spp strains.
Published
Feb 10, 2025
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Melissa Arango-Gil
https://orcid.org/0009-0004-2337-1442
Marcela Mora-López
https://orcid.org/0000-0002-7706-0883
Elizabeth Correa-Gómez
https://orcid.org/0000-0001-7659-7518
Victor Manuel Osorio-Echeverri
https://orcid.org/0000-0002-9134-2713
https://orcid.org/0009-0004-2337-1442
Marcela Mora-López
https://orcid.org/0000-0002-7706-0883
Elizabeth Correa-Gómez
https://orcid.org/0000-0001-7659-7518
Victor Manuel Osorio-Echeverri
https://orcid.org/0000-0002-9134-2713
##plugins.themes.bootstrap3.article.details##
Abstract
Most fungal infections are caused by species of the Candida genus, particularly C. albicans. The increasing number of strains developing resistance to antifungals, resulting in treatment failures, underscores the urgency of finding new antifungal agents. Since many bacteria of the genus Streptomyces produce molecules that inhibit fungal growth, this work aimed to evaluate the antifungal activity of three native isolates obtained from a rhizosphere and an artisanal composting system. Based on 16S RNA gene sequences, as well as biochemical and morphological traits, we identified S. globisporus, S. bacillaris, and S. cavourensis as the species most closely related to the S1H, S40, and S41 isolates, respectively. These species have been reported to produce antifungal compounds. The inhibition of Candida by antagonistic activity increased with longer Streptomyces incubation times, with no differences observed between Candida species. Few studies have simultaneously evaluated the inhibitory activity of Streptomyces isolates against different Candida strains. In this study, the isolates inhibited the growth of C. albicans, C. krusei, C. guilliermondii, C. glabrata, and C. lusitaniae, including strains resistant to fluconazole.
Keywords
actinobacteria, antagonism, antifungal activity, antimicrobial-resistant fungi, pathogenic yeasts, native microorganisms.
References
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https://doi.org/10.2174/1389203720666190722152415
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https://doi.org/10.3390/jof6010015
[6] Bongomin F, Gago S, Oladele RO, Denning DW. Global and multi-national prevalence of fungal diseases -estimate precision, Journal of Fungi, 3(4): 57, 2017.
https://doi.org/10.3390/jof3040057
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https://doi.org/10.1016/j.riam.2016.02.006
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https://doi.org/10.7705/biomedica.4400
[9] Gómez-Gaviria M, Mora-Montes HM. Current aspects in the biology, pathogeny, and treatment of Candida krusei, a neglected fungal pathogen, Infection and Drug Resistance, 13: 1673–1689, 2020.
https://doi.org/10.2147/IDR.S247944
[10] Naicker SD, Shuping L, Zulu TG, Mpembe RS, Mhlanga M, Tsotetsi EM, Maphanga TG, Govender NP. Epidemiology and susceptibility of Nakaseomyces (formerly Candida) glabrata bloodstream isolates from hospitalised adults in South Africa. Medical Mycology,
61(6): myad057, 2023.
https:/doi.org/10.1093/mmy/myad057
[11] Ahangarkani F, Badali H, Rezai MS, Shokohi T, Abtahian Z, Mahmoodi Nesheli H, Karami H, Roilides E, Tamaddoni A. Candidemia due to Candida guilliermondii in an immunocompromised infant: a case report and review of literature, Current Medical
Mycology, 5(1): 32–36, 2019.
https://doi.org/10.18502/cmm.5.1.535
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https://doi.org/10.7759/cureus.43211
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https://doi.org/10.3390/jof8101077
[14] Panariello BHD, Klein MI, Mima EGDO, PavarinaAC. Fluconazole impacts the extracellular matrix of fluconazole-susceptible and -resistant Candida albicans and Candida glabrata biofilms, Journal of Oral Microbiology, 10: 1476644, 2018.
https://doi.org/10.1080/20002297.2018.1476644
[15] Kordalewska M, Zhao Y, Lockhart SR, Chowdhary A, Berrio I, Perlin DS. Rapid and accurate molecular identification of the emerging multidrug-resistant pathogen Candida auris, Journal of Clinical Microbiology, 55(8): 2445–2452, 2017.
https://doi.org/10.1128/JCM.00630-17
[16] Donadu MG, Peralta-Ruiz Y, Usai D, Maggio F, Molina-Hernandez JB, Rizzo D, Bussu F, Rubino S, Zanetti S, Paparella A, Chaves-Lopez C. Colombian essential oil of Ruta graveolens against nosocomial antifungal resistant Candida strains, Journal of Fungi, 7(5):
383, 2021.
https://doi.org/10.3390/jof7050383
[17] Donald L, Pipite A, Subramani R, Owen J, Keyzers RA, Taufa T. Streptomyces: Still the biggest producer of new natural secondary metabolites, a current perspective, Microbiology Research, 13(3): 418–465, 2022.
https://doi.org/10.3390/microbiolres13030031
[18] Huang K, Zhang B, Shen ZY, Cai X, Liu ZQ, Zheng YG. Enhanced amphotericin B production by genetically engineered Streptomyces nodosus, Microbiological Research, 242: 126623, 2021.
https://doi.org/10.1016/j.micres.2020.126623
[19] Liu R, Deng Z, Liu, T. Streptomyces species: Ideal chassis for natural product discovery and overproduction, Metabolic Engineering, 50: 74–84, 2018.
https://doi.org/10.1016/j.ymben.2018.05.015
[20] Bontemps C, Toussaint M, Revol PV, Hotel L, Jeanbille M, Uroz S, Turpault MP, Blaudez D, Leblond P. Taxonomic and functional diversity of Streptomyces in a forest soil, FEMS Microbiology Letters, 342(2): 157–167, 2013.
https://doi.org/10.1111/1574-6968.12126
[21] Khamna S, Yokota A, Lumyong S. Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production, World Journal of Microbiology and Biotechnology, 25: 649-655, 2009.
https://doi.org/10.1007/s11274-008-9933-x
[22] Law JWF, Pusparajah P, Ab Mutalib NS,Wong SH, Goh BH, Lee LH. A review on mangrove actinobacterial diversity: The roles of Streptomyces and novel species discovery, Progress in Microbes and Molecular Biology, 2(1): a0000024, 2019.
[23] Ryckeboer J, Mergaert J, Coosemans J, Deprins K, Swings J. Microbiological aspects of biowaste during composting in a monitored compost bin, Journal of Applied Microbiology, 94(1): 127-137, 2003.
https://doi.org/10.1046/j.1365-2672.2003.01800.x
[24] Ayed A, Essid R, Jallouli S, Zaied AB, Fdhila SB, Limam F, Tabbene O. Antifungal activity of volatile organic compounds (VOCs) produced by Streptomyces olivochromogenes S103 against Candida albicans, Euro-Mediterranean Journal for Environmental Integration, 7(2): 251–255, 2022.
https://doi.org/10.1007/s41207-022-00302-w
[25] Chen C, Chen X, Ren B, Guo H, Abdel-Mageed WM, Liu X, Song F, Zhang, L. Characterization of Streptomyces sp. LS462 with high productivity of echinomycin, a potent antituberculosis and synergistic antifungal antibiotic, Journal of Industrial Microbiology and Biotechnology, 48: 9–10, 2021.
https://doi.org/10.1093/jimb/kuab079
[26] Ministerio de Salud y Protección Social República de Colombia. Resolución 1411 de 2022 por la cual se adopta la Política de Soberanía en la producción para la Seguridad Sanitaria.
https://www.minsalud.gov.co/Normatividad_Nuevo/Resoluci%C3%B3n%20No.%201411%20de%202022.pdf.
[27] Kämpfer P. Order XIV. Streptomycetales ord. nov. In M Goodfellow, P Kämpfer, HJ Busse, ME Trujillo, K Suzuki, W Ludwig, WB Whitman (ed.), Bergey’s Manual of Systematic Bacteriology. Volume 5. The Actinobacteria, Part A and B. 2nd ed. Springer, Athens, USA.
2012.
[28] Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species, International Journal of Systematic Bacteriology, 16(3): 313–340, 1966.
https://doi.org/10.1099/00207713-16-3-313
[29] Sharma D, Kaur T, Chadha BS, Manhas RK. Antimicrobial activity of actinomycetes against multidrug resistant Staphylococcus aureus, E. coli and various other pathogens, Tropical Journal of Pharmaceutical Research, 10(6): 801–808, 2011.
https://doi.org/10.4314/tjpr.v10i6.14
[30] Lane D. 16S/23S rRNA sequencing. In E Stackebrandt, M Goodfellow (ed.), Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons, New York, USA. 1991.
[31] Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of
sequence data, Bioinformatics, 28(12): 1647–1649, 2012.
https://doi.org/10.1093/bioinformatics/bts199
[32] Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Research, 22(22): 4673–4680, 1994.
https://doi.org/10.1093/nar/22.22.4673
[33] Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool, Journal of Molecular Biology, 215(3): 403–410, 1990.
https://doi.org/10.1016/S0022-2836(05)80360-2
[34] Clinical and Laboratory Standards Institute – CLSI. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. 4th ed. CLSI Standard M27. Clinical and Laboratory Standards Institute, Wayne, PA, USA. 2017.
[35] Velho-Pereira S, Kamat NM. Antimicrobial screening of actinobacteria using a modified cross-streak method, Indian Journal of Pharmaceutical Sciences, 73(2): 223–228, 2011.
https://doi.org/10.4103/0250-474x.91566
[36] Cuesta G, García-de-la-Fuente R, Abad M, Fornes F. Isolation and identification of actinomycetes from a compost-amended soil with potential as biocontrol agents, Journal of Environmental Management, 95: S280–S284, 2012.
https://doi.org/10.1016/j.jenvman.2010.11.023
[37] Devi P, Sujatha K, Chendrayan K, Sivakumar U. Laccase producing Streptomyces bikiniensis CSC12 isolated from compost, Journal of Microbiology, Biotechnology and Food Sciences, 6(2): 794–798, 2016.
https://doi.org/10.15414/jmbfs.2016.6.2.794-798
[38] Ekundayo FO, Oyeniran KA, Adedokun AD. Antimicrobial activities of some Streptomyces isolated from garden soil samples and fish pond water in FUTA, Journal of Bio-Science, 22: 21–29, 2014.
https://doi.org/10.3329/jbs.v22i0.30005
[39] Kelly KL, Judd DB. Color. Universal Language and Dictionary of Names. Washington, DC: National Bureau of Standards. 1955.
[40] Centore P. ISCC-NBS Colour System. 2016.
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How to Cite
Arango-Gil , M., Mora-López , M., Correa-Gómez , E., & Osorio-Echeverri, V. M. (2025). Characterization of three native Streptomyces isolates that inhibit the growth of fluconazole-resistant Candida spp strains. Universitas Scientiarum, 30, 1–20. https://doi.org/10.11144/Javeriana.SC30.cotn
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Applied Microbiology
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