The potency of Actinomycetes InaCC A758 against dual-species biofilms: Candida albicans and Staphylococcus aureus

Setiawati Setiawati Eti Nurwening Sholikah Titik Nuryastuti Jumina Jumina Puspita Lisdiyanti Mustofa Mustofa   

Open Access   

Published:  Jun 10, 2024

DOI: 10.7324/JAPS.2024.144035
Abstract

Candida albicans and Staphylococcus aureus can coexist to form a biofilm, leading to infections associated with biofilms. Actinomycetes produce secondary metabolites known as antibiotics, antifungals, antibiofilm, anticancer, and antimalarials. This study was aimed to explore the antibiofilm activity of secondary metabolites of Actinomycetes InaCC A758 extracts (InaCC A758) against dual-species biofilms, i.e., C. albicans and S. aureus. Ethyl acetate and chloroform were used as solvents in a maceration extraction technique to isolate the compound designated InaCC A758. The fractionation of the InaCC A758 extracts was carried out using semi-preparative HPLC. Identification of the compounds from the InaCC A758 extracts was performed using gas chromatography-mass spectrometry analysis. Antimicrobial and antibiofilm testing of the InaCC A758 extracts was done utilizing the micro broth dilution method. The morphology of the biofilms following treatment with the InaCC A758 extracts was visualized using scanning electron microscopy (SEM). The minimum inhibitory concentration of InaCC A758 against dual-species biofilms was 400 μg/ml. The concentrations of InaCC A758 required to inhibit 50% and 80% of dual-species biofilm formation (BIC50 and BIC80) ranged from 3.57–6.66 and 29.25–30.50 μg/ml, respectively. The concentrations needed to reduce formed dual-species biofilms by 50% and 80% (BRC50 and BRC80) ranged from 100.62–131.85 and 596.4–849.6 μg/ml, respectively. SEM observation showed a reduced number of cells and disruption of the cell membranes when exposed to the InaCC A758 extracts. The InaCC A758 contains seven compounds, i.e., dodecanoic acid 3-hydroxy-; 1,3,5-pentanetriol,3-methyl-; 1,3-dioxolane-4-methanol, 2-ethyl-; 2-cyclopropylcarbonyloxytridecane; 2-hepten-1- ol,(E); methyl 6-methyl heptanoate; and 11-octadecenoic acid, methyl ester. The InaCC A758 extract altered cell morphology and exhibited potential as an anti-biofilm agent, particularly against dual-species biofilms.


Keyword:     Actinomycetes extract antibiofilm dual-species Candida albicans Staphylococcus aureus


Citation:

Setiawati S, Sholikah EN, Nuryastuti T, Jumina J, Lisdiyanti P, Mustofa M. The potency of Actinomycetes InaCC A758 against dual-species biofilms: Candida albicans and Staphylococcus aureus. J Appl Pharm Sci. 2024. Online First. http://doi.org/10.7324/JAPS.2024.144035

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Reference

1 Pammi M, Zhong D, Johnson Y, Revell P, Versalovic J. Polymicrobial bloodstream infections in the neonatal intensive care unit are associated with increased mortality: a case-control study. BMC Infect Dis. 2014;14:1–8. doi: https://doi.org/10.1186/1471-2334-14-390

2. Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW, Shirtliff ME. Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol. 2010;59:493–503. doi: https://doi.org/10.1111/j.1574-695X.2010.00710.x

3. Yang L, Liu Y, Wu H, Høiby N, Molin S, Song Z. Current understanding of multi-species biofilms. Int J Oral Sci. 2011;3:74–81. doi: https://doi.org/10.4248/IJOS11027

4. Klotz SA, Chasin BS, Powell B, Gaur NK, Lipke PN. Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. Diagn Microbiol Infect Dis. 2007;59:401–6. doi: https://doi.org/10.1016/j.diagmicrobio.2007.07.001

5. Harriott MM, Noverr MC. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother. 2009;53:3914–22. doi: https://doi.org/10.1128/AAC.00657-09

6. Dumitru R, Hornby JM, Kenneth W, Nickerson KW. Defined anaerobic growth medium for studying Candida albicans basic biology and resistance to eight antifungal drugs. Antimicrob Agents Chemother. 2004;48:2350–4. doi: https://doi.org/10.1128/AAC.48.7.2350

7. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum M, et al. Biofilm formation by the fungal pathogen Candida albicans: development, architecture and drug resistance. Natl Rev Microbiol. 2001;183:5385–94. doi: https://doi.org/10.1128/JB.183.18.5385

8. Khanna N. Antimicrobial agents: antifungal & antiviral drugs. Delhi, India: University College of Medical Sciences Shahdara; 2007.

9. Larabi M, Legrand P, Appel M, Gil S, Lepoivre M, Devissaguet JP, et al. Reduction of NO synthase expression and tumor necrosis factor alpha production in macrophages by amphotericin B lipid carriers. Antimicrob Agents Chemother. 2001;45:553–62. doi: https://doi.org/10.1128/AAC.45.2.553-562.2001

10. Dodds Ashley ES, Lewis R, Lewis JS, Martin C, Andes D. Pharmacology of systemic antifungal agents. Clin Infect Dis. 2006;43:S28–39. doi: https://doi.org/10.1086/504492

11. Ambavane V, Tokdar P, Parab R, Sreekumar ES, Mahajan G, Mishra PD, et al. Caerulomycin a—an antifungal compound isolated from marine actinomycetes. Adv Microbiol. 2014;04:567–78. doi: https://doi.org/10.4236/aim.2014.49063

12. Belghit S, Driche EH, Bijani C, Zitouni A, Sabaou N, Badji B, et al. Activity of 2,4-di-tert-butylphenol produced by a strain of Streptomyces mutabilis isolated from a Saharan soil against Candida albicans and other pathogenic fungi. J Mycol Med. 2016;26:160–9. doi: https://doi.org/10.1016/j.mycmed.2016.03.001

13. Nithyanand P, Thenmozhi R, Rathna J, Karutha Pandian S. Inhibition of Streptococcus pyogenes biofilm formation by coral-associated actinomycetes. Curr Microbiol. 2010;60:454–60. doi: https://doi.org/10.1007/s00284-009-9564-y

14. Guo Y, Wei C, Liu C, Li D, Sun J, Huang H, et al. Inhibitory effects of oral Actinomyces on the proliferation, virulence and biofilm formation of Candida albicans. Arch Oral Biol. 2015;60:1368–74. doi: https://doi.org/10.1016/j.archoralbio.2015.06.015

15. Setiawati S, Nuryastuti T, Sholikhah ETIN. The potency of actinomycetes extracts isolated from Pramuka Island, Jakarta, Indonesia as antimicrobial agents. Biodiversitas. 2021;22:1104–11. doi: https://doi.org/10.13057/biodiv/d220304

16. Setiawati S, Nuryastuti T, Ngatidjan N, Mustofa M, Jumina J, Fitriastuti D. In vitro antifungal activity of (1)-N-2-methoxybenzyl-1,10-phenanthrolinium bromide against Candida albicans and its effects on membrane integrity. Mycobiology. 2017;45:25–30. doi: https://doi.org/10.5941/MYCO.2017.45.1.25

17. Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Wayne, PA: CLSI; 2015. doi: https://doi.org/10.4103/0976-237X.91790

18. Kart D, Tavernier S, Acker H Van, Nelis HJ, Coenye T. Activity of disinfectants against multispecies biofilms formed by Staphylococcus aureus, Candida albicans and Pseudomonas aeruginosa. Biofouling. 2014;30:377–83. doi: https://doi.org/10.1080/08927014.2013.8783331

19. Taff HT, Mitchell KF, Edward JA, Andes DR. Mechanisms of Candida biofilm drug resistance. Future Microbiol. 2013;8:1325–37. doi: https://doi.org/10.2217/fmb.13.101

20. Wang D, Wang C, Gui P, Liu H, Khalaf SMH, Elsayed EA, et al. Identification, bioactivity, and productivity of actinomycins from the marine-derived Streptomyces heliomycini. Front Microbiol. 2017;8:1–12. doi: https://doi.org/10.3389/fmicb.2017.01147

21. Torex A, Sasidharan S. Anti-Candida albicans biofilm activity by Cassia spectabilis standardized methanol extract: an ultrastructural study. Eur Rev Med Pharmacol Sci. 2011;15:875–82.

22. Tsang PWK, Bandara HMHN, Fong WP. Purpurin suppresses Candida albicans biofilm formation and hyphal development. PLoS One. 2012;7:1–8. doi: https://doi.org/10.1371/journal.pone.0050866

23. Wu P-S, Kuo Y-T, Chen S, Li Y, Lou B-S. Gas chromatography-mass spectrometry analysis of photosensitive characteristics in citrus and herb essential oils. J Chromatogr Sep Tech. 2014;6:1–9. doi: https://doi.org/10.4172/2157-7064.1000261

24. Carolus H, Van Dyck K, Van Dijck P. Candida albicans and Staphylococcus species: a threatening twosome. Front Microbiol. 2019;10:2162. doi: https://doi.org/10.3389/fmicb.2019.02162

25. Todd OA, Fidel PL, Harro JM, Hilliard JJ, Tkaczyk C, Sellman BR, et al. Candida albicans augments Staphylococcus aureus virulence by engaging the staphylococcal agr quorum sensing system. MBio. 2019;10:1–16. doi: https://doi.org/10.1128/mBio.00910-19

26. Sudbery P, Gow N, Berman J. The distinct morphogenic states of Candida albicans. Trends Microbiol. 2004;12:317–24. doi: https://doi.org/10.1016/j.tim.2004.05.008

27. Kong EF, Kucharíková S, Van Dijck P, Peters BM, Shirtliff ME, Jabra-Rizka MA. Clinical implications of oral candidiasis: host tissue damage and disseminated bacterial disease. Infect Immun. 2015;83:604–13. doi: https://doi.org/10.1128/IAI.02843-14

28. Peters BM, Ovchinnikova ES, Krom BP, Schlecht LM, Zhou H, Hoyer LL, et al. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology (United Kingdom). 2012;158:2975–86. doi: https://doi.org/10.1099/mic.0.062109-0

29. Kean R, Rajendran R, Haggarty J, Townsend EM, Short B, Burgess KE, et al. Candida albicans mycofilms support Staphylococcus aureus colonization and enhances miconazole resistance in dual-species interactions. Front Microbiol. 2017;8:1–11. doi: https://doi.org/10.3389/fmicb.2017.00258

30. Dharni S, Gupta S, Maurya A, Samad A, Srivastava SK, Sharma A, et al. Purification, characterization and in vitro activity of 2, 4-di-tert-butylphenol from Pseudomonas monteilii PsF84: conformational and molecular docking studies. J Agric Food Chem. 2014;62(26):6138–46.

31. Padmavathi AR, Abinaya B, Pandian SK. Phenol, 2,4-bis(1,1-dimethylethyl) of marine bacterial origin inhibits quorum sensing mediated biofilm formation in the uropathogen Serratia marcescens. Biofouling. 2014;30:1111–22. doi: https://doi.org/10.1080/08927014.2014.972386

32. Kiran GS, Sabarathnam B, Selvin J. Biofilm disruption potential of a glycolipid biosurfactant from marine Brevibacterium casei. FEMS Immunol Med Microbiol. 2010;59:432–8. doi: https://doi.org/10.1111/j.1574-695X.2010.00698.x

33. Desbois AP, Smith VJ. Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. App Micobiol Biotechnol. 2010;85:1629–42. doi: https://doi.org/10.1007/s00253-009-2355-3

34. Kumar P, Lee J, Beyenal H, Lee J. Fatty acids as antibiofilm and antivirulence agents. Trends Microbiol. 2020;28:1–16. doi: https://doi.org/10.1016/j.tim.2020.03.014

35. Kim Y, Lee J, Raorane CJ, Oh ST, Park JG, Lee J, et al. Herring oil and omega fatty acids inhibit Staphylococcus aureus biofilm formation and virulence. Front Microbiol. 2018;9:1–10. doi: https://doi.org/10.3389/fmicb.2018.01241

36. Wenderska IB, Chong M, Mcnulty J, Wright GD. Palmitoyl-DL-carnitine is a multitarget inhibitor of Pseudomonas aeruginosa biofilm development. Chembiochem. 2011;12:2759–66. doi: https://doi.org/10.1002/cbic.201100500

37. Prasath KG, Sethupathy S, Pandian SK. Proteomic analysis uncovers the modulation of ergosterol, sphingolipid and oxidative stress pathway by myristic acid impeding biofilm and virulence in Candida albicans. J Proteomics. 2019;208:103503. doi: https://doi.org/10.1016/j.jprot.2019.103503

38. Lee J, Kim Y, Kiran S, Lee J. Antibiofilm and antifungal activities of medium-chain fatty acids against Candida albicans via mimicking of the quorum-sensing molecule farnesol. Microb Biotechnol. 2020;14(4):1353–66. doi: https://doi.org/10.1111/1751-7915.13710

39. Dixit AK, Kumar V, Maloni N, Sarkar M, Shrivastava B, Nair PG, et al. Comparative assessment of phytochemicals, antioxidant, and antimicrobial potential of stem bark and small branches of Buchanania cochinchinensis (Lour.). J Drug Res Ayuverdic Sci. 2019;4(2):72–8.doi: https://doi.org/10.5005/jp-journals-10059-0069

40. Kucuk H, Yusufoglu A, Mataraci E, Dosler S. Synthesis and biological activity of new 1,3-dioxolanes as potential antibacterial and antifungal compounds. Moleculs. 2011;16(8):6806–15. doi: https://doi.org/10.3390/molecules16086806

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