A Potent Antifungal Activity by the Marine Streptomyces albidoflavus sp. ADR10 from the Caspian Sea Sediment: Optimization and Primary Purification

Document Type : Research Article

Authors

1 Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

2 Department of Chemistry, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

Abstract

Fungal infections are an evolving public health challenge due to their antimicrobial resistance and the growth of immunocompromised populations. Aquatic environments, the largest ecosystem on earth, are recently considered as a source for the production of bioactive compounds. Marine actinomycetes are considered for their potential to produce novel bioactive metabolites like antifungal compounds. In this study, strain ADR10 was obtained from the sediment sample of the Caspian Sea and its 16S rDNA gene sequence analysis suggested that the isolate belongs to Streptomyces albidoflavus. The preliminary cross-streak and double-layer agar screening revealed that the isolate has potent activity against pathogenic fungi, i.e. Aspergillus niger, Candida albicans, Fusarium oxysporum, and Penicillium crustosum. One-factor-at-a-time and Response surface methodology (RSM) was employed to evaluate the effects of six parameters (carbon source, initial pH, inoculation volume, NaCl concentration, nitrogen source, and temperature) on the production of antibiotics in the basal starch casein broth medium. The maximum antibiotic activity was achieved at the initial pH 7.05, sucrose 1.17 g l-1, malt 0.2 g l-1, temperature 30 ºC, inoculation size 5.0% v/v, and NaCl 1% w/v after 121.1 hours. Through the optimization experiments, antifungal activity was enhanced 2.7-fold.  Ethyl acetate showed the highest antibiotic extraction capacity from the fermentation media compared with dichloromethane, hexane, and chloroform. The preliminary purified antibiotic by thin layer chromatography (ethyl acetate/ mobile petroleum phase) showed a more significant growth inhibition zone than nystatin (100 μg mL-1) against Candida albicans. This study underlines the potential of the marine actinomycete for the identification of novel antifungal agents.

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References

Asolkar, R. N., Jensen, P. R., Kauffman, C. A., & Fenical, W. (2006). Daryamides A- C, weakly cytotoxic polyketides from a marine-derived actinomycete of the genus Streptomyces strain CNQ-085. Journal of Natural Products, 69(12), 1756-1759. https://doi.org/10.1021/np0603828
Augustine, S. K., Bhavsar, S. P., & Kapadnis, B. P. (2005). A non-polyene antifungal antibiotic from Streptomyces albidoflavus PU 23. Journal of Biosciences, 30(2), 201-211. https://doi.org/10.1007/BF02703700
Badiee, P., & Hashemizadeh, Z. (2014). Opportunistic invasive fungal infections: diagnosis & clinical management. Indian Journal of Medical Research, 139(2), 195-204. https://journals.lww.com/ijmr/toc/2014/39020
Balouiri, M., Sadiki, M., & Ibnsouda, S. K. (2016). Methods for in vitro evaluating antimicrobial activity: A review. Journal of Pharmaceutical Analysis, 6(2), 71-79. https://doi.org/10.1016/j.jpha.2015.11.005
Box G. E. P., & Behnken, D. W. 1960. Some new three level designs for the study of quantitative variables. Technometrics 2: 455-475.https://www.tandfonline.com/doi/abs/10.1080/00401706.1960.10489912
Carlucci, A., Raimondo, M. L., Colucci, D., & Lops, F. (2022). Streptomyces albidoflavus Strain CARA17 as a biocontrol agent against fungal soil-borne pathogens of fennel plants. Plants 11(11), 1420.  https://doi.org/10.3390/plants11111420
Chen, C., Wang, Y., Su, C., Zhao, X., Li, M., Meng, X., ... & Suh, J. W. (2015). Antifungal activity of Streptomyces albidoflavus L131 against the leaf mold pathogen Passalora fulva involves membrane leakage and oxidative damage. Journal of the Korean Society for Applied Biological Chemistry, 58, 111-119. https://doi.org/10.1007/s13765-015-0012-3
Cho, K. W., Seo, Y. W., Yoon, T. M., & Shin, J. H. (1999). Purification and structure determination of antifungal phospholipids from a marine Streptomyces. Journal of Microbiology and Biotechnology, 9(6), 709-715. https://sciwatch.kiost.ac.kr/handle/2020.kiost/6133
Dalisay, D. S., Williams, D. E., Wang, X. L., Centko, R., Chen, J., & Andersen, R. J. (2013). Marine sediment-derived Streptomyces bacteria from British Columbia, Canada are a promising microbiota resource for the discovery of antimicrobial natural products. PLoS One, 8(10), e77078. https://doi.org/10.1371/journal.pone.0077078
De La Hoz-Romo, M. C., Díaz, L., & Villamil, L. (2022). Marine actinobacteria a new source of antibacterial metabolites to treat acne vulgaris disease- a systematic literature review. Antibiotics, 11(7), 965. https://doi.org/10.3390/antibiotics11070965
de Simeis, D., & Serra, S. (2021). Actinomycetes: a never-ending source of bioactive compounds- an overview on antibiotics production. Antibiotics, 10(5), 483. https://doi.org/10.3390/antibiotics10050483
Islam, M. R., Jeong, Y. T., Ryu, Y. J., Song, C. H., & Lee, Y. S. (2009). Isolation, identification and optimal culture conditions of Streptomyces albidoflavus C247 producing antifungal agents against Rhizoctonia solani AG2-2. Mycobiology, 37(2), 114-120. https://doi.org/10.4489/MYCO.2009.37.2.114
Kagan, I. A., & Flythe, M. D. (2014). Thin-layer chromatographic (TLC) separations and bioassays of plant extracts to identify antimicrobial compounds. Journal of Visualized Experiments, (85), e51411. https://doi.org/10.3791/51411
Kolesnichenko, I. V., Goloverda, G. Z., & Kolesnichenko, V. L. (2019). A versatile method of ambient-temperature solvent removal. Organic Process Research and Development, 24(1), 25-31.  https://doi.org/10.1021/acs.oprd.9b00368
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7):1870-4. https://doi.org/ 10.1093/molbev/msw054
Lane DJ, Pace B, Olsen GJ, Stahl D, Sogin M, Pace NR. 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proceedings of the National Academy of Sciences of the United States of America 82: 6955-59. https://doi.org/ 10.1073/pnas.82.20.6955
Leroy, S. A., Marret, F., Gibert, E., Chalié, F., Reyss, J. L., & Arpe, K. (2007). River inflow and salinity changes in the Caspian Sea during the last 5500 years. Quaternary Science Reviews, 26(25-28), 3359-3383. https://doi.org/10.1016/j.quascirev.2007.09.012
Mahmoudi, N., Robeson, M. S., Castro, H. F., Fortney, J. L., Techtmann, S. M., Joyner, D. C., ... & Hazen, T. C. (2015). Microbial community composition and diversity in Caspian Sea sediments. FEMS Microbiology Ecology, 91(1), 1-11. https://doi.org/10.1093/femsec/fiu013
Makhdoumi, A. (2018). Bacterial diversity in south coast of the Caspian Sea: Culture-dependent and culture-independent survey. Caspian Journal of Environmental Sciences, 16(3), 259-269. https://doi.org/10.22124/CJES.2018.3066
Mehrshad, M., Amoozegar, M. A., Ghai, R., Shahzadeh Fazeli, S. A., & Rodriguez-Valera, F. (2016). Genome reconstruction from metagenomic data sets reveals novel microbes in the brackish waters of the Caspian sea. Applied and Environmental Microbiology, 82(5), 1599-1612. https://doi.org/10.1128/AEM.03381-15
Nobile, C. J., & Johnson, A. D. (2015). Candida albicans biofilms and human disease. Annual Review of Microbiology, 69, 71-92. https://doi.org/10.1146/annurev-micro-091014-104330
Ossai, J., Khatabi, B., Nybo, S. E., & Kharel, M. K. (2022). Renewed interests in the discovery of bioactive actinomycete metabolites driven by emerging technologies. Journal of Applied Microbiology, 132(1), 59-77.  https://doi.org/10.1111/jam.15225
Rajan, B. M., & Kannabiran, K. (2014). Extraction and identification of antibacterial secondary metabolites from marine Streptomyces sp. VITBRK2. International Journal of Molecular and Cellular Medicine, 3(3), 130-137. http://ijmcmed.org/article-1-179-en.html
Saraswathi, K., Mahalakshmi, S., Khusro, A., Arumugam, P., Mohammed, A. K., & Alkufeidy, R. M. (2020). In vitro biological properties of Streptomyces cangkringensis isolated from the floral rhizosphere regions. Saudi Journal of Biological Sciences, 27(12), 3249-3257. https://doi.org/10.1016/j.sjbs.2020.09.035
Schwarz, J., Hubmann, G., Rosenthal, K., & Lütz, S. (2021). Triaging of culture conditions for enhanced secondary metabolite diversity from different bacteria. Biomolecules, 11(2), 193. https://doi.org/10.3390/biom11020193
Stachurska, X., Roszak, M., Jabłońska, J., Mizielińska, M., & Nawrotek, P. (2021). Double-layer agar (DLA) modifications for the first step of the phage-antibiotic synergy (PAS) identification. Antibiotics, 10(11), 1306.https://doi.org/10.3390/antibiotics10111306
Souagui, S., Djoudi, W., Boudries, H., Béchet, M., Leclère, V., & Kecha, M. (2019). Modeling and statistical optimization of culture conditions for improvement of antifungal compounds production by Streptomyces albidoflavus S19 strain of wastewater origin. Anti-infective Agents, 17(1), 39-49.  https://doi.org/10.2174/2211352516666180813102424
Wang, Y. H., Feng, J. T., Zhang, Q., & Zhang, X. (2008). Optimization of fermentation condition for antibiotic production by Xenorhabdus nematophila with response surface methodology. Journal of Applied Microbiology, 104(3), 735-744. https://doi.org/10.1111/j.1365-2672.2007.03599.x
Yun, T. Y., Feng, R. J., Zhou, D. B., Pan, Y. Y., Chen, Y. F., Wang, F., ... & Xie, J. H. (2018). Optimization of fermentation conditions through response surface methodology for enhanced antibacterial metabolite production by Streptomyces sp. 1-14 from cassava rhizosphere. PloS One, 13(11), e0206497. https://doi.org/10.1371/journal.pone.0206497
Zhang, D., Yi, W., Ge, H., Zhang, Z., & Wu, B. (2019). Bioactive streptoglutarimides A-J from the marine-derived Streptomyces sp. ZZ741. Journal of Natural Products, 82(10), 2800-2808. https://doi.org/10.1021/acs.jnatprod.9b00481
Journal of Genetic Resources
Volume 9, Issue 2
2023
Pages 151-160

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