Antifungal effect of soil Bacillus bacteria on pathogenic species of the fungal genera Aspergillus and Trichophyton
-
Mahnour Alsadat Taghavi
,
Maryam Ahmadi
,
Davoud Dehghan-Nayeri
,
Zahra Salehi
,
Masoomeh Shams-Ghahfarokhi
,
Fatemehsadat Jamzivar
,
Mehdi Razzaghi-Abyaneh
Abstract
Background and Objectives: The increasing prevalence of fungal infections due to antifungal resistance underscores the need for novel treatment strategies. The present study aimed to investigate the inhibitory effects of soil-originated antagonistic bacteria against Aspergillus and Trichophyton species.
Materials and Methods: Fifty soil samples collected from Isfahan and Khuzestan provinces by using the Zig-Zag method were cultured on glucose-yeast extract (GY) agar around fungal colonies to isolate antagonistic bacteria. Antifungal activity was assessed by measuring clear zones around the colonies of A. niger, A. fumigatus, T. rubrum, and T. mentagrophytes by co-culture linear method. Potent antagonistic bacteria were identified by 16S rRNA sequencing, and evaluated for antifungal activity using disk diffusion assays compared with amphotericin B and ketoconazole.
Results: Among 50 samples, fifteen showed antifungal effects, yielding 55 bacterial strains. Four isolates with strong antifungal activity against all tested fungi were identified as Bacillus subtilis, B. licheniformis, B. axarquiensis, and Bacillus sp. These bacteria were distributed in distinct clusters phylogenitically and showed diverse antifungal activity.
Conclusion: The results suggest the potential of soil-derived Bacillus species as promising antifungal agents. Further studies are recommended to identify their inhibitory metabolites, their ability as biocontrol agents against soil habitated fungi and to explore their mechanism of action and spectrum of activity.
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23. Ciesielska A, Kawa A, Kanarek K, Soboń A, Szewczyk R. Metabolomic analysis of Trichophyton rubrum and Microsporum canis during keratin degradation. Sci Rep 2021; 11: 3959.
24. Gnat S, Łagowski D, Nowakiewicz A, Osińska M, Kopiński Ł. Population differentiation, antifungal susceptibility, and host range of Trichophyton mentagrophytes isolates causing recalcitrant infections in humans and animals. Eur J Clin Microbiol Infect Dis 2020; 39: 2099-2113.
25. Paiva Macedo JD, Dias VC. Antifungal resistance: why are we losing this battle? Future Microbiol 2024; 19: 1027-1040.
26. Gupta AK, Mann A, Polla Ravi S, Wang T. An update on antifungal resistance in dermatophytosis. Expert Opin Pharmacother 2024; 25: 511-519.
27. Kim PI, Ryu JW, Kim YH, Chi YT. Production of biosurfactant lipopeptides iturin A, fengycin, and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 2010; 20: 138-145.
28. Ramachandran R, Shrivastava M, Narayanan NN, Thakur RL, Chakrabarti A, Roy U. Evaluation of antifungal efficacy of three new cyclic lipopeptides of the class bacillomycin from Bacillus subtilis RLID 12.1. Antimicrob Agents Chemother 2017; 62(1): e01457-17.
29. Tunsagool P, Ploypetch S, Jaresitthikunchai J, Roytrakul S, Choowongkomon K, Rattanasrisomporn J. Efficacy of cyclic lipopeptides obtained from Bacillus subtilis to inhibit the growth of Microsporum canis isolated from cats. Heliyon 2021; 7(9): e07980.
30. Lei S, Zhao H, Pang B, Qu R, Lian Z, Jiang C, et al. Capability of iturin from Bacillus subtilis to inhibit Candida albicans in vitro and in vivo. Appl Microbiol Biotechnol 2019; 103: 4377-4392.
31. Subramenium GA, Swetha TK, Iyer PM, Balamurugan K, Pandian SK. 5-hydroxymethyl-2-furaldehyde from marine bacterium Bacillus subtilis inhibits biofilm and virulence of Candida albicans. Microbiol Res 2018; 207: 19-32.
32. Bais HP, Fall R, Vivanco JM. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 2004; 134: 307-319.
2. Wiederhold NP. Antifungal resistance: current trends and future strategies to combat. Infect Drug Resist 2017; 10: 249-259.
3. Berman J, Krysan DJ. Drug resistance and tolerance in fungi. Nat Rev Microbiol 2020; 18: 319-331.
4. Beardsley J, Halliday CL, Chen SCA, Sorrell TC. Responding to the emergence of antifungal drug resistance: perspectives from the bench and the bedside. Future Microbiol 2018; 13: 1175-1191.
5. Vandeputte P, Ferrari S, Coste AT. Antifungal resistance and new strategies to control fungal infections. Int J Microbiol 2012; 2012: 713687.
6. Sharrar AM, Crits-Christoph A, Méheust R, Diamond S, Starr EP, Banfield JF, et al. Bacterial secondary metabolite biosynthetic potential in soil varies with phylum, depth, and vegetation type. mBio 2020; 11(3): e00416-20.
7. Amin M, Rakhisi Z, Zarei Ahmady A. Isolation and identification of Bacillus species from soil and evaluation of their antibacterial properties. Avicenna J Clin Microbiol Infect 2015; 2: 23233.
8. Stein T. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 2005; 56: 845-857.
9. Caulier S, Nannan C, Gillis A, Licciardi F, Bragard C, Mahillon J. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front Microbiol 2019; 10: 302.
10. Dunlap CA, Bowman MJ, Rooney AP. Iturinic lipopeptide diversity in the Bacillus subtilis species group: important antifungals for plant disease biocontrol applications. Front Microbiol 2019; 10: 1749.
11. Caulier S, Gillis A, Colau G, Licciardi F, Liépin M, Desoignies N, et al. Versatile antagonistic activities of soil-borne Bacillus spp. and Pseudomonas spp. against Phytophthora infestans and other potato pathogens. Front Microbiol 2018; 9: 143.
12. Alamri SA. Enhancing the efficiency of the bioagent Bacillus subtilis JF419701 against soil-borne phytopathogens by increasing the productivity of fungal cell wall degrading enzymes. Arch Phytopathol Plant Prot 2014; 48: 159-170.
13. Jafari S, Aghaei SS, Afifi-Sabet H, Shams-Ghahfarokhi M, Jahanshiri Z, Gholami-Shabani M, et al. Exploration, antifungal and antiaflatoxigenic activity of halophilic bacteria communities from saline soils of Howze-Soltan playa in Iran. Extremophiles 2018; 22: 87-98.
14. Ranjbariyan A, Shams-Ghahfarokhi M, Kalantari S, Razzaghi-Abyaneh M. Molecular identification of antagonistic bacteria from Tehran soils and evaluation of their inhibitory activities toward pathogenic fungi. Iran J Microbiol 2011; 3: 140-156.
15. Shams-Ghahfarokhi M, Kalantari S, Razzaghi-Abyaneh M (2013). Terrestrial Bacteria from agricultural soils: versatile weapons against aflatoxigenic fungi. In: Razzaghi-Abyaneh M (ed) Aflatoxins: Recent Advances and Future Prospects. InTech, Rijeka.
16. Gebily DA, Ghanem GA, Ragab MM, Ali AM, Soliman NEK, El-Moity A, et al. Characterization and potential antifungal activities of three Streptomyces spp. as biocontrol agents against Sclerotinia sclerotiorum infecting green beans. Egypt J Biol Pest Control 2021; 31: 1-15.
17. Mohammadi R, Abbaszadeh S, Sharifzadeh A, Sepandi M, Taghdir M, Youseftabar Miri N, et al. In vitro activity of encapsulated lactic acid bacteria on aflatoxin production and growth of Aspergillus spp. Food Sci Nutr 2021; 9: 1282-1288.
18. Bidaud A-L, Schwarz P, Herbreteau G, Dannaoui E. Techniques for the assessment of in vitro and in vivo antifungal combinations. J Fungi (Basel) 2021; 7: 113.
19. Paulussen C, Hallsworth JE, Álvarez-Pérez S, Nierman WC, Hamill PG, Blain D, et al. Ecology of aspergillosis: insights into the pathogenic potency of Aspergillus fumigatus and some other Aspergillus species. Microb Biotechnol 2017; 10: 296-322.
20. Boral H, Metin B, Döğen A, Seyedmousavi S, Ilkit M. Overview of selected virulence attributes in Aspergillus fumigatus, Candida albicans, Cryptococcus neoformans, Trichophyton rubrum, and Exophiala dermatitidis. Fungal Genet Biol 2018; 111: 92-107.
21. Pinto E, Monteiro C, Maia M, Faria MA, Lopes V, Lameiras C, et al. Aspergillus species and antifungal susceptibility in clinical settings in the North of Portugal: cryptic species and emerging azoles resistance in A. fumigatus. Front Microbiol 2018; 9: 1656.
22. Gautier M, Normand AC, Ranque S. Previously unknown species of Aspergillus. Clin Microbiol Infect 2016; 22: 662-669.
23. Ciesielska A, Kawa A, Kanarek K, Soboń A, Szewczyk R. Metabolomic analysis of Trichophyton rubrum and Microsporum canis during keratin degradation. Sci Rep 2021; 11: 3959.
24. Gnat S, Łagowski D, Nowakiewicz A, Osińska M, Kopiński Ł. Population differentiation, antifungal susceptibility, and host range of Trichophyton mentagrophytes isolates causing recalcitrant infections in humans and animals. Eur J Clin Microbiol Infect Dis 2020; 39: 2099-2113.
25. Paiva Macedo JD, Dias VC. Antifungal resistance: why are we losing this battle? Future Microbiol 2024; 19: 1027-1040.
26. Gupta AK, Mann A, Polla Ravi S, Wang T. An update on antifungal resistance in dermatophytosis. Expert Opin Pharmacother 2024; 25: 511-519.
27. Kim PI, Ryu JW, Kim YH, Chi YT. Production of biosurfactant lipopeptides iturin A, fengycin, and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 2010; 20: 138-145.
28. Ramachandran R, Shrivastava M, Narayanan NN, Thakur RL, Chakrabarti A, Roy U. Evaluation of antifungal efficacy of three new cyclic lipopeptides of the class bacillomycin from Bacillus subtilis RLID 12.1. Antimicrob Agents Chemother 2017; 62(1): e01457-17.
29. Tunsagool P, Ploypetch S, Jaresitthikunchai J, Roytrakul S, Choowongkomon K, Rattanasrisomporn J. Efficacy of cyclic lipopeptides obtained from Bacillus subtilis to inhibit the growth of Microsporum canis isolated from cats. Heliyon 2021; 7(9): e07980.
30. Lei S, Zhao H, Pang B, Qu R, Lian Z, Jiang C, et al. Capability of iturin from Bacillus subtilis to inhibit Candida albicans in vitro and in vivo. Appl Microbiol Biotechnol 2019; 103: 4377-4392.
31. Subramenium GA, Swetha TK, Iyer PM, Balamurugan K, Pandian SK. 5-hydroxymethyl-2-furaldehyde from marine bacterium Bacillus subtilis inhibits biofilm and virulence of Candida albicans. Microbiol Res 2018; 207: 19-32.
32. Bais HP, Fall R, Vivanco JM. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 2004; 134: 307-319.
| Files | ||
| Issue | Vol 17 No 2 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i2.18397 | |
| Keywords | ||
| Antifungal activity; Aspergillus; Trichophyton; Bacillus; Molecular identification; Soil bacteria | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Taghavi M, Ahmadi M, Dehghan-Nayeri D, Salehi Z, Shams-Ghahfarokhi M, Jamzivar F, Razzaghi-Abyaneh M. Antifungal effect of soil Bacillus bacteria on pathogenic species of the fungal genera Aspergillus and Trichophyton. Iran J Microbiol. 2025;17(2):303-311.
