The Potency of Soil Actinomycetes Extracts as Antibiofilm Agents against Enterococcus faecalis
Keywords:
Enterococcus faecalis, biofilm, antibacterial, antibiofilm, Actinomycetes
Abstract
Background. Enterococcus faecalis is a bacterium often found in root canal infections. Its virulence and biofilm formation can cause persistent apical periodontitis. Actinomycetes are Gram-positive bacteria known to produce a wide variety of novel biologically active compounds, including antibacterial, antitumor, immunosuppressive agents, and enzyme inhibitors. This study aimed to determine the potency of Actinomycetes extracts from Gunungkidul and Pontianak soil, Indonesia, as antibiofilm agents against E. faecalis and to identify the possible related primary compounds present in the active extracts.
Materials and Methods. Actinomycetes extracts, Streptomyces sp. GMR22 (from Gunungkidul) and Streptomyces sp. ACT214 (from Pontianak) were tested for its antibacterial and antibiofilm activity against E. faecalis through microbroth dilution assay and scanning electron microscopy (SEM) imaging. Primary compounds present in the active extracts were analyzed using untargeted liquid chromatography-tandem high-resolution mass spectrometry (LC-HRMS).
Results. Streptomyces sp. ACT214 demonstrated potent antibacterial activity with a minimum inhibitory concentration (MIC) of 1,250 ppm and a minimum bactericidal concentration (MBC) of 5,000 ppm. Otherwise, GMR22 did not reach MIC or MBC at the highest concentration tested (5,000 ppm). Streptomyces sp. ACT214 also exhibited concentration-dependent antibiofilm effects, fully preventing E. faecalis biofilm formation at 582 ppm (MBIC90) and disrupting biofilm formation under SEM observation. In contrast, GMR22 showed a lower inhibition effect.
Conclusion. This result suggests that Actinomycetes extract from Pontianak soil, Indonesia has potential as an antibiofilm agent against E. faecalis. As a potential source of new antibiotic compounds, these soil Actinomycetes extracts warrant further exploration as alternative treatments targeting E. faecalis biofilm in recalcitrant apical periodontitis cases.
References
Abd El-Aleam, R. H., George, R. F., Georgey, H. H., & Abdel-Rahman, H. M. (2021). Bacterial virulence factors: A target for heterocyclic compounds to combat bacterial resistance. RSC Advances, 11(58), 36459–36482. https://doi.org/10.1039/d1ra06238g
Abouelhassan, Y., Garrison, A. T., Burch, G. M., Wong, W., Norwood, V. M., & Huigens, R. W. (2014). Discovery of quinoline small molecules with potent dispersal activity against methicillin-resistant Staphylococcus aureus and Staphylococcus epidermidis biofilms using a scaffold hopping strategy. Bioorganic and Medicinal Chemistry Letters, 24(21), 5076–5080. https://doi.org/10.1016/j.bmcl.2014.09.009
Alghamdi, F., & Shakir, M. (2020). The influence of Enterococcus faecalis as a dental root canal pathogen on endodontic treatment: A systematic review. Cureus, 12(3), e7257. https://doi.org/10.7759/cureus.7257
Ali, I. A. A., Matinlinna, J. P., Lévesque, C. M., & Neelakantan, P. (2021). Trans-cinnamaldehyde attenuates Enterococcus faecalis virulence and inhibits biofilm formation. Antibiotics, 10(6), 702. https://doi.org/10.3390/antibiotics10060702
Al-Madi, E. M., Almohaimede, A. A., Al-Obaida, M. I., & Awaad, A. S. (2019). Comparison of the antibacterial efficacy of commiphora molmol and sodium hypochlorite as root canal irrigants against Enterococcus faecalis and Fusobacterium nucleatum. Evidence-Based Complementary and Alternative Medicine, 2019(4), 1-6. https://doi.org/10.1155/2019/6916795
Almeida, N. L. M., Saldanha, L. L., da Silva, R. A., Pinke, K. H., da Costa, E. F., Porto, V. C., Dokkedal, A. L., & Lara, V. S. (2018). Antimicrobial activity of denture adhesive associated with Equisetum giganteumand Punica granatum-enriched fractions against Candida albicans biofilms on acrylic resin surfaces. Biofouling, 34(1), 62–73. https://doi.org/10.1080/08927014.2017.1407408
Barka, E. A., Vatsa, P., Sanchez, L., Gaveau-Vaillant, N., Jacquard, C., Klenk, H.-P., Clément, C., Ouhdouch, Y., & van Wezel, G. P. (2016). Taxonomy, Physiology, and Natural Products of Actinobacteria. Microbiology and Molecular Biology Reviews, 80(1), 1–43. https://doi.org/10.1128/mmbr.00019-15
Davies, D. G., & Marques, C. N. H. (2009). A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. Journal of Bacteriology, 191(5), 1393–1403. https://doi.org/10.1128/JB.01214-08
Dioguardi, M., Di Gioia, G., Illuzzi, G., Arena, C., Caponio, V. C. A., Caloro, G. A., Zhurakivska, K., Adipietro, I., Troiano, G., & Lo Muzio, L. (2019). Inspection of the microbiota in endodontic lesions. Dentistry journal, 7(2), 47. https://doi.org/10.3390/dj7020047
Ferreira, M., Pinto, S. N., Aires‐da‐silva, F., Bettencourt, A., Aguiar, S. I., & Gaspar, M. M. (2021). Liposomes as a nanoplatform to improve the delivery of antibiotics into staphylococcus aureus biofilms. Pharmaceutics, 13(3), 1–25. https://doi.org/10.3390/pharmaceutics13030321
Ghaly, M. F., Albalawi, M. A., Bendary, M. M., Shahin, A., Shaheen, M. A., Abu Eleneen, A. F., Ghoneim, M. M., Elmaaty, A. A., Elrefai, M. F. M., Zaitone, S. A., & Abousaty, A. I. (2023). Tamarindus indica extract as a promising antimicrobial and antivirulence Therapy. Antibiotics, 12(3). https://doi.org/10.3390/antibiotics12030464
Hussein, H. H., Abood, F. M., & Alhelal, A. G. (2020). Some virulence factors of Enterococcus faecalis isolated from root canal infections combined with effect of some irrigation solution against E. faecalis. Systematic Reviews in Pharmacy, 11(6), 742–748. https://doi.org/10.31838/srp.2020.6.109
Jakubiec-Krzesniak, K., Rajnisz-Mateusiak, A., Guspiel, A., Ziemska, J., & Solecka, J. (2018). Secondary metabolites of Actinomycetes and their antibacterial, antifungal and antiviral properties. Polish journal of microbiology, 67(3), 259–272. https://doi.org/10.21307/pjm-2018-048
Jalaluldeen, A. M., Sijam, K., Othman, R., Abidin, Z., & Ahmad, M. (2015). Growth characteristics and production of secondary metabolites from selected Streptomyces species isolated from the Rhizosphere of Chili Plant. International Journal of Enhanced Research in Science Technology & Engineering, 4(1): 1-8.
Jin, X., Zhou, J., Richey, G., Wang, M., Choi Hong, S. M., & Hong, S. H. (2021). Undecanoic acid, lauric acid, and N-tridecanoic acid inhibit Escherichia coli persistence and biofilm formation. Journal of Microbiology and Biotechnology, 31(1), 130–136. https://doi.org/10.4014/JMB.2008.08027
Kamarudheen, N., & Rao, K. V. B. (2019). Fatty acyl compounds from marine Streptomyces griseoincarnatus strain HK12 against two major bio-film forming nosocomial pathogens; an in vitro and in silico approach. Microbial Pathogenesis, 127, 121–130. https://doi.org/10.1016/j.micpath.2018.11.050
Khadke, S. K., Lee, J. H., Kim, Y. G., Raj, V., & Lee, J. (2021). Assessment of antibiofilm potencies of nervonic and oleic acid against Acinetobacter baumannii using in vitro and computational approaches. Biomedicines, 9(9). https://doi.org/10.3390/biomedicines9091133
Khalifa, L., Shlezinger, M., Beyth, S., Houri-Haddad, Y., Coppenhagen-Glazer, S., Beyth, N., & Hazan, R. (2016). Phage therapy against Enterococcus faecalis in dental root canals. Journal of oral microbiology, 8, 32157. https://doi.org/10.3402/jom.v8.32157
Khattab, A. I., Babiker, E. H., & Saeed, H. A. (2016). Streptomyces: isolation, optimization of culture conditions and extraction of secondary metabolites. International Current Pharmaceutical Journal, 5(3), 27–32. https://doi.org/10.3329/icpj.v5i3.26695
Kim, M. A., Rosa, V., & Min, K. S. (2020). Characterization of Enterococcus faecalis in different culture conditions. Scientific Reports, 10(1), 21867. https://doi.org/10.1038/s41598-020-78998-5
Kumar, P., Lee, J. H., Beyenal, H., & Lee, J. (2020). Fatty acids as antibiofilm and antivirulence agents. Trends in microbiology, 28(9), 753–768. https://doi.org/10.1016/j.tim.2020.03.014
Lee, J. H., Kim, Y. G., Shim, S. H., & Lee, J. (2017). Antibiofilm activities of norharmane and its derivatives against Escherichia coli O157:H7 and other bacteria. Phytomedicine, 36, 254–261. https://doi.org/10.1016/j.phymed.2017.10.013
Li, S., Chan, K. K. wan, Hua, M. Z., Gölz, G., & Lu, X. (2022). Inhibition of AI-2 quorum sensing and biofilm formation in Campylobacter jejuni by decanoic and lauric acids. Frontiers in microbiology, 12, 811506. https://doi.org/10.3389/fmicb.2021.811506
Liu, R. H., Shang, Z. C., Li, T. X., Yang, M. H., & Kong, L. Y. (2017). In vitro antibiofilm activity of eucarobustol E against Candida albicans. Antimicrobial agents and chemotherapy, 61(8), e02707-16. https://doi.org/10.1128/AAC.02707-16
Liu, Y., Su, S., Yu, M., Zhai, D., Hou, Y., Zhao, H., Ma, X., Jia, M., Xue, X., & Li, M. (2022). Pyrancoumarin derivative LP4C targeting of pyrimidine de novo synthesis pathway inhibits MRSA biofilm and virulence. Frontiers in pharmacology, 13, 959736. https://doi.org/10.3389/fphar.2022.959736
Low, C. F., Shamsir, M. S., Mohamed-Hussein, Z. A., & Baharum, S. N. (2019). Evaluation of potential molecular interaction between quorum sensing receptor, LuxP and grouper fatty acids: In-silico screening and simulation. PeerJ, 7, e6568. https://doi.org/10.7717/peerj.6568
Luz, L. B., Santana, R., Prates, A. W., Froelich, J., De Melo, T. A. F., Montagner, F., & Luisi, S. B. (2019). Antimicrobial action, pH, and tissue dissolution capacity of 2.5% sodium hypochlorite gel and solution. Journal of Health & Biological Sciences, 7(2(Abr-Jun)), 121–125. https://doi.org/10.12662/2317-3076jhbs.v7i2.2327.p121-125.2019
Martínez, E., Cosnahan, R. K., Wu, M., Gadila, S. K., Quick, E. B., Mobley, J. A., & Campos-Gómez, J. (2019). Oxylipins mediate cell-to-cell communication in Pseudomonas aeruginosa. Communications Biology, 2(1). https://doi.org/10.1038/s42003-019-0310-0
Melinda, Y. N., Widada, J., Wahyuningsih, T. D., Febriansah, R., Damayanti, E., & Mustofa, M. (2021). Metabologenomics approach to the discovery of novel compounds from Streptomyces sp. GMR22 as anti-SARS-CoV-2 drugs. Heliyon, 7(11). e08308. https://doi.org/10.1016/j.heliyon.2021.e08308
Miller, T., Waturangi, D. E., & Yogiara. (2022). Antibiofilm properties of bioactive compounds from Actinomycetes against foodborne and fish pathogens. Scientific Reports, 12(1), 18614. https://doi.org/10.1038/s41598-022-23455-8
Nicol, M., Alexandre, S., Luizet, J. B., Skogman, M., Jouenne, T., Salcedo, S. P., & Dé, E. (2018). Unsaturated fatty acids affect quorum sensing communication system and inhibit motility and biofilm formation of Acinetobacter baumannii. International Journal of Molecular Sciences, 19(1), 214. https://doi.org/10.3390/ijms19010214
Nirwati, H., Damayanti, E., Sholikhah, E. N., Mutofa, M., & Widada, J. (2022). Soil-derived Streptomyces sp. GMR22 producing antibiofilm activity against Candida albicans: bioassay, untargeted LC-HRMS, and gene cluster analysis. Heliyon, 8(4), e09333. https://doi.org/10.1016/j.heliyon.2022.e09333
Oja, T., Galindo, P. S. M., Taguchi, T., Manner, S., Vuorela, P. M., Ichinose, K., Metsä-Ketelä, M., & Fallarero, A. (2015). Effective antibiofilm polyketides against Staphylococcus aureus from the pyranonaphthoquinone biosynthetic pathways of Streptomyces species. Antimicrobial Agents and Chemotherapy, 59(10), 6046–6052. https://doi.org/10.1128/AAC.00991-15
Peeters, E., Nelis, H. J., & Coenye, T. (2008). Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. Journal of Microbiological Methods, 72(2), 157–165. https://doi.org/10.1016/j.mimet.2007.11.010
Purbowati, R., Pratiwi, V. M., Masfufatun, M., Tania, P. O. A., & Khumaeni, A. (2023). Antibacterial and antibiofilm effects of gold and silver nanoparticles against the uropathogenic Escherichia coli by scanning electron microscopy (SEM) analysis. Healthcare in Low-Resource Settings, 11(2). https://doi.org/10.4081/hls.2023.11748
Raissa, G., Waturangi, D. E., & Wahjuningrum, D. (2020). Screening of antibiofilm and anti-quorum sensing activty of Actinomycetes isolates extracts against aquaculture pathogenic bacteria. BMC Microbiology, 20(1), 343. https://doi.org/10.1186/s12866-020-02022-z
Reen, F. J., Gutiérrez-Barranquero, J. A., Parages, M. L., & O’Gara, F. (2018). Coumarin: a novel player in microbial quorum sensing and biofilm formation inhibition. Applied microbiology and biotechnology, 102(5), 2063–2073. https://doi.org/10.1007/s00253-018-8787-x
Ruli Tambunan, T., Widada, J., Damayanti, E., & Dwi Wahyuningsih, T. (2020). Antiplasmodial activity of the low molecular weight compounds from Streptomyces sp. GMR22. Indonesian Journal of Pharmacy, 31(4), 273-280. https://www.swissadme.ch
Saigal, Irfan, M., Khan, P., Abid, M., & Khan, M. M. (2019). Design, synthesis, and biological evaluation of novel fused Spiro-4 H-pyran derivatives as bacterial biofilm disruptor. ACS Omega, 4(16), 16794–16807. https://doi.org/10.1021/acsomega.9b01571
Saito, H. E., Harp, J. R., & Fozo, E. M. (2014). Incorporation of exogenous fatty acids protects Enterococcus faecalis from membrane-damaging agents. Applied and Environmental Microbiology, 80(20), 6527–6538. https://doi.org/10.1128/AEM.02044-14
Seguel, N., Quezada-Aguiluz, M., González-Rocha, G., Bello-Toledo, H., & Sánchez-Sanhueza, G. (2020). Antibiotic resistance of Enterococcus faecalis from persistent endodontic infections. International Journal of. Odontostomatology, 14(3). 448-456.
Seipke, R. F. (2015). Strain-level diversity of secondary metabolism in Streptomyces albus. PLoS ONE, 10(1). e0116457. https://doi.org/10.1371/journal.pone.0116457
Senerovic, L., Opsenica, D., Moric, I., Aleksic, I., Spasić, M., & Vasiljevic, B. (2020). Quinolines and quinolones as antibacterial, antifungal, anti-virulence, antiviral and anti-parasitic agents. Advances in experimental medicine and biology, 1282, 37–69. https://doi.org/10.1007/5584_2019_428
Setiawati, S., & Yusan, R. T. (2022). Actinomycetes as a source of potential antimicrobial and antibiofilm agents. Medical and Health Journal, 1(2), 50. https://doi.org/10.20884/1.mhj.2022.1.2.5831
She, P., Wang, Y., Li, Y., Zhou, L., Li, S., Zeng, X., Liu, Y., Xu, L., & Wu, Y. (2021). Drug repurposing: in vitro and in vivo antimicrobial and antibiofilm effects of bithionol against Enterococcus faecalis and Enterococcus faecium. Frontiers in Microbiology, 12. 579806. https://doi.org/10.3389/fmicb.2021.579806
Sottorff, I., Wiese, J., Lipfert, M., Preußke, N., Sönnichsen, F. D., & Imhoff, J. F. (2019). Different secondary metabolite profiles of phylogenetically almost identical Streptomyces griseus strains originating from geographically remote locations. Microorganisms, 7(6), 166. https://doi.org/10.3390/microorganisms7060166
Stenz, L., François, P., Fischer, A., Huyghe, A., Tangomo, M., Hernandez, D., Cassat, J., Linder, P., & Schrenzel, J. (2008). Impact of oleic acid (cis-9-octadecenoic acid) on bacterial viability and biofilm production in Staphylococcus aureus. FEMS Microbiology Letters, 287(2), 149–155. https://doi.org/10.1111/j.1574-6968.2008.01316.x
Stuart, C., Schwartz, S., Beeson, T., & Owatz, C. (2006). Enterococcus faecalis: Its role in root canal treatment failure and current concepts in retreatment. Journal of Endodontics, 32(2), 93–98. https://doi.org/10.1016/j.joen.2005.10.049
Su, S., Yin, P., Li, J., Chen, G., Wang, Y., Qu, D., Li, Z., Xue, X., Luo, X., & Li, M. (2020). In vitro and in vivo anti-biofilm activity of pyran derivative against Staphylococcus aureus and Pseudomonas aeruginosa. Journal of Infection and Public Health, 13(5), 791–799. https://doi.org/10.1016/j.jiph.2019.10.010
Suhartono, S., Soraya, C., & Shabira, P. (2023). Antibiofilm activity of neem leaf (Azadirachta indica A. Juss) ethanolic extracts against Enterococcus faecalis in vitro. Dental Journal, 56(2), 98–103. https://doi.org/10.20473/J.DJMKG.V56.I2.P98-103
Wang, Q. Q., Zhang, C. F., Chu, C. H., & Zhu, X. F. (2012). Prevalence of Enterococcus faecalis in saliva and filled root canals of teeth associated with apical periodontitis. International Journal of Oral Science, 4(1), 19–23. https://doi.org/10.1038/ijos.2012.17
Waturangi, D. E., Rahayu, B. S., Lalu, K. Y., Michael, & Mulyono, N. (2016). Characterization of bioactive compound from Actinomycetes for antibiofilm activity against Gram-negative and Gram-positive bacteria. Malaysian Journal of Microbiology, 12(4), 291–299. https://doi.org/10.21161/mjm.80915
Windaryanti, D., Gabriel, C. S., Hidayat, I. W., Zainuddin, A., Dharsono, H. D. A., Satari, M. H., & Kurnia, D. (2022). The potential of 24-propylcholestrol as antibacterial oral bacteria of Enterococcus faecalis ATCC 29212 and inhibitor biofilms formation: in vitro and in silico study. Advances and Applications in Bioinformatics and Chemistry, 15, 99–111. https://doi.org/10.2147/AABC.S372337
Wong, J., Manoil, D., Näsman, P., Belibasakis, G. N., & Neelakantan, P. (2021). Microbiological aspects of root canal infections and disinfection strategies: an update review on the current knowledge and challenges. Frontiers in Oral Health, 2, 672887. https://doi.org/10.3389/froh.2021.672887
Xie, T. T., Zeng, H., Ren, X. P., Wang, N., Chen, Z. J., Zhang, Y., & Chen, W. (2019). Antibiofilm activity of three Actinomycete strains against Staphylococcus epidermidis. Letters in applied microbiology, 68(1), 73–80. https://doi.org/10.1111/lam.13087
Ye, L., Cao, L., Song, W., Yang, C., Tang, Q., & Yuan, Z. (2023). Interaction between apical periodontitis and systemic disease (Review). International Journal of Molecular Medicine, 52(1), 60. https://doi.org/10.3892/ijmm.2023.5263
Yuyama, K. T., Rohde, M., Molinari, G., Stadler, M., & Abraham, W. R. (2020). Unsaturated fatty acids control biofilm formation of Staphylococcus aureus and other Gram-positive bacteria. Antibiotics, 9(11), 1–11. https://doi.org/10.3390/antibiotics9110788
Zeng, X., She, P., Zhou, L., Li, S., Hussain, Z., Chen, L., & Wu, Y. (2021). Drug repurposing: Antimicrobial and antibiofilm effects of penfluridol against Enterococcus faecalis. MicrobiologyOpen, 10(1), e1148. https://doi.org/10.1002/mbo3.1148
Zoletti, G. O., Pereira, E. M., Schuenck, R. P., Teixeira, L. M., Siqueira, J. F., & dos Santos, K. R. N. (2011). Characterization of virulence factors and clonal diversity of Enterococcus faecalis isolates from treated dental root canals. Research in Microbiology, 162(2), 151–158. https://doi.org/10.1016/j.resmic.2010.09.018
Abouelhassan, Y., Garrison, A. T., Burch, G. M., Wong, W., Norwood, V. M., & Huigens, R. W. (2014). Discovery of quinoline small molecules with potent dispersal activity against methicillin-resistant Staphylococcus aureus and Staphylococcus epidermidis biofilms using a scaffold hopping strategy. Bioorganic and Medicinal Chemistry Letters, 24(21), 5076–5080. https://doi.org/10.1016/j.bmcl.2014.09.009
Alghamdi, F., & Shakir, M. (2020). The influence of Enterococcus faecalis as a dental root canal pathogen on endodontic treatment: A systematic review. Cureus, 12(3), e7257. https://doi.org/10.7759/cureus.7257
Ali, I. A. A., Matinlinna, J. P., Lévesque, C. M., & Neelakantan, P. (2021). Trans-cinnamaldehyde attenuates Enterococcus faecalis virulence and inhibits biofilm formation. Antibiotics, 10(6), 702. https://doi.org/10.3390/antibiotics10060702
Al-Madi, E. M., Almohaimede, A. A., Al-Obaida, M. I., & Awaad, A. S. (2019). Comparison of the antibacterial efficacy of commiphora molmol and sodium hypochlorite as root canal irrigants against Enterococcus faecalis and Fusobacterium nucleatum. Evidence-Based Complementary and Alternative Medicine, 2019(4), 1-6. https://doi.org/10.1155/2019/6916795
Almeida, N. L. M., Saldanha, L. L., da Silva, R. A., Pinke, K. H., da Costa, E. F., Porto, V. C., Dokkedal, A. L., & Lara, V. S. (2018). Antimicrobial activity of denture adhesive associated with Equisetum giganteumand Punica granatum-enriched fractions against Candida albicans biofilms on acrylic resin surfaces. Biofouling, 34(1), 62–73. https://doi.org/10.1080/08927014.2017.1407408
Barka, E. A., Vatsa, P., Sanchez, L., Gaveau-Vaillant, N., Jacquard, C., Klenk, H.-P., Clément, C., Ouhdouch, Y., & van Wezel, G. P. (2016). Taxonomy, Physiology, and Natural Products of Actinobacteria. Microbiology and Molecular Biology Reviews, 80(1), 1–43. https://doi.org/10.1128/mmbr.00019-15
Davies, D. G., & Marques, C. N. H. (2009). A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. Journal of Bacteriology, 191(5), 1393–1403. https://doi.org/10.1128/JB.01214-08
Dioguardi, M., Di Gioia, G., Illuzzi, G., Arena, C., Caponio, V. C. A., Caloro, G. A., Zhurakivska, K., Adipietro, I., Troiano, G., & Lo Muzio, L. (2019). Inspection of the microbiota in endodontic lesions. Dentistry journal, 7(2), 47. https://doi.org/10.3390/dj7020047
Ferreira, M., Pinto, S. N., Aires‐da‐silva, F., Bettencourt, A., Aguiar, S. I., & Gaspar, M. M. (2021). Liposomes as a nanoplatform to improve the delivery of antibiotics into staphylococcus aureus biofilms. Pharmaceutics, 13(3), 1–25. https://doi.org/10.3390/pharmaceutics13030321
Ghaly, M. F., Albalawi, M. A., Bendary, M. M., Shahin, A., Shaheen, M. A., Abu Eleneen, A. F., Ghoneim, M. M., Elmaaty, A. A., Elrefai, M. F. M., Zaitone, S. A., & Abousaty, A. I. (2023). Tamarindus indica extract as a promising antimicrobial and antivirulence Therapy. Antibiotics, 12(3). https://doi.org/10.3390/antibiotics12030464
Hussein, H. H., Abood, F. M., & Alhelal, A. G. (2020). Some virulence factors of Enterococcus faecalis isolated from root canal infections combined with effect of some irrigation solution against E. faecalis. Systematic Reviews in Pharmacy, 11(6), 742–748. https://doi.org/10.31838/srp.2020.6.109
Jakubiec-Krzesniak, K., Rajnisz-Mateusiak, A., Guspiel, A., Ziemska, J., & Solecka, J. (2018). Secondary metabolites of Actinomycetes and their antibacterial, antifungal and antiviral properties. Polish journal of microbiology, 67(3), 259–272. https://doi.org/10.21307/pjm-2018-048
Jalaluldeen, A. M., Sijam, K., Othman, R., Abidin, Z., & Ahmad, M. (2015). Growth characteristics and production of secondary metabolites from selected Streptomyces species isolated from the Rhizosphere of Chili Plant. International Journal of Enhanced Research in Science Technology & Engineering, 4(1): 1-8.
Jin, X., Zhou, J., Richey, G., Wang, M., Choi Hong, S. M., & Hong, S. H. (2021). Undecanoic acid, lauric acid, and N-tridecanoic acid inhibit Escherichia coli persistence and biofilm formation. Journal of Microbiology and Biotechnology, 31(1), 130–136. https://doi.org/10.4014/JMB.2008.08027
Kamarudheen, N., & Rao, K. V. B. (2019). Fatty acyl compounds from marine Streptomyces griseoincarnatus strain HK12 against two major bio-film forming nosocomial pathogens; an in vitro and in silico approach. Microbial Pathogenesis, 127, 121–130. https://doi.org/10.1016/j.micpath.2018.11.050
Khadke, S. K., Lee, J. H., Kim, Y. G., Raj, V., & Lee, J. (2021). Assessment of antibiofilm potencies of nervonic and oleic acid against Acinetobacter baumannii using in vitro and computational approaches. Biomedicines, 9(9). https://doi.org/10.3390/biomedicines9091133
Khalifa, L., Shlezinger, M., Beyth, S., Houri-Haddad, Y., Coppenhagen-Glazer, S., Beyth, N., & Hazan, R. (2016). Phage therapy against Enterococcus faecalis in dental root canals. Journal of oral microbiology, 8, 32157. https://doi.org/10.3402/jom.v8.32157
Khattab, A. I., Babiker, E. H., & Saeed, H. A. (2016). Streptomyces: isolation, optimization of culture conditions and extraction of secondary metabolites. International Current Pharmaceutical Journal, 5(3), 27–32. https://doi.org/10.3329/icpj.v5i3.26695
Kim, M. A., Rosa, V., & Min, K. S. (2020). Characterization of Enterococcus faecalis in different culture conditions. Scientific Reports, 10(1), 21867. https://doi.org/10.1038/s41598-020-78998-5
Kumar, P., Lee, J. H., Beyenal, H., & Lee, J. (2020). Fatty acids as antibiofilm and antivirulence agents. Trends in microbiology, 28(9), 753–768. https://doi.org/10.1016/j.tim.2020.03.014
Lee, J. H., Kim, Y. G., Shim, S. H., & Lee, J. (2017). Antibiofilm activities of norharmane and its derivatives against Escherichia coli O157:H7 and other bacteria. Phytomedicine, 36, 254–261. https://doi.org/10.1016/j.phymed.2017.10.013
Li, S., Chan, K. K. wan, Hua, M. Z., Gölz, G., & Lu, X. (2022). Inhibition of AI-2 quorum sensing and biofilm formation in Campylobacter jejuni by decanoic and lauric acids. Frontiers in microbiology, 12, 811506. https://doi.org/10.3389/fmicb.2021.811506
Liu, R. H., Shang, Z. C., Li, T. X., Yang, M. H., & Kong, L. Y. (2017). In vitro antibiofilm activity of eucarobustol E against Candida albicans. Antimicrobial agents and chemotherapy, 61(8), e02707-16. https://doi.org/10.1128/AAC.02707-16
Liu, Y., Su, S., Yu, M., Zhai, D., Hou, Y., Zhao, H., Ma, X., Jia, M., Xue, X., & Li, M. (2022). Pyrancoumarin derivative LP4C targeting of pyrimidine de novo synthesis pathway inhibits MRSA biofilm and virulence. Frontiers in pharmacology, 13, 959736. https://doi.org/10.3389/fphar.2022.959736
Low, C. F., Shamsir, M. S., Mohamed-Hussein, Z. A., & Baharum, S. N. (2019). Evaluation of potential molecular interaction between quorum sensing receptor, LuxP and grouper fatty acids: In-silico screening and simulation. PeerJ, 7, e6568. https://doi.org/10.7717/peerj.6568
Luz, L. B., Santana, R., Prates, A. W., Froelich, J., De Melo, T. A. F., Montagner, F., & Luisi, S. B. (2019). Antimicrobial action, pH, and tissue dissolution capacity of 2.5% sodium hypochlorite gel and solution. Journal of Health & Biological Sciences, 7(2(Abr-Jun)), 121–125. https://doi.org/10.12662/2317-3076jhbs.v7i2.2327.p121-125.2019
Martínez, E., Cosnahan, R. K., Wu, M., Gadila, S. K., Quick, E. B., Mobley, J. A., & Campos-Gómez, J. (2019). Oxylipins mediate cell-to-cell communication in Pseudomonas aeruginosa. Communications Biology, 2(1). https://doi.org/10.1038/s42003-019-0310-0
Melinda, Y. N., Widada, J., Wahyuningsih, T. D., Febriansah, R., Damayanti, E., & Mustofa, M. (2021). Metabologenomics approach to the discovery of novel compounds from Streptomyces sp. GMR22 as anti-SARS-CoV-2 drugs. Heliyon, 7(11). e08308. https://doi.org/10.1016/j.heliyon.2021.e08308
Miller, T., Waturangi, D. E., & Yogiara. (2022). Antibiofilm properties of bioactive compounds from Actinomycetes against foodborne and fish pathogens. Scientific Reports, 12(1), 18614. https://doi.org/10.1038/s41598-022-23455-8
Nicol, M., Alexandre, S., Luizet, J. B., Skogman, M., Jouenne, T., Salcedo, S. P., & Dé, E. (2018). Unsaturated fatty acids affect quorum sensing communication system and inhibit motility and biofilm formation of Acinetobacter baumannii. International Journal of Molecular Sciences, 19(1), 214. https://doi.org/10.3390/ijms19010214
Nirwati, H., Damayanti, E., Sholikhah, E. N., Mutofa, M., & Widada, J. (2022). Soil-derived Streptomyces sp. GMR22 producing antibiofilm activity against Candida albicans: bioassay, untargeted LC-HRMS, and gene cluster analysis. Heliyon, 8(4), e09333. https://doi.org/10.1016/j.heliyon.2022.e09333
Oja, T., Galindo, P. S. M., Taguchi, T., Manner, S., Vuorela, P. M., Ichinose, K., Metsä-Ketelä, M., & Fallarero, A. (2015). Effective antibiofilm polyketides against Staphylococcus aureus from the pyranonaphthoquinone biosynthetic pathways of Streptomyces species. Antimicrobial Agents and Chemotherapy, 59(10), 6046–6052. https://doi.org/10.1128/AAC.00991-15
Peeters, E., Nelis, H. J., & Coenye, T. (2008). Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. Journal of Microbiological Methods, 72(2), 157–165. https://doi.org/10.1016/j.mimet.2007.11.010
Purbowati, R., Pratiwi, V. M., Masfufatun, M., Tania, P. O. A., & Khumaeni, A. (2023). Antibacterial and antibiofilm effects of gold and silver nanoparticles against the uropathogenic Escherichia coli by scanning electron microscopy (SEM) analysis. Healthcare in Low-Resource Settings, 11(2). https://doi.org/10.4081/hls.2023.11748
Raissa, G., Waturangi, D. E., & Wahjuningrum, D. (2020). Screening of antibiofilm and anti-quorum sensing activty of Actinomycetes isolates extracts against aquaculture pathogenic bacteria. BMC Microbiology, 20(1), 343. https://doi.org/10.1186/s12866-020-02022-z
Reen, F. J., Gutiérrez-Barranquero, J. A., Parages, M. L., & O’Gara, F. (2018). Coumarin: a novel player in microbial quorum sensing and biofilm formation inhibition. Applied microbiology and biotechnology, 102(5), 2063–2073. https://doi.org/10.1007/s00253-018-8787-x
Ruli Tambunan, T., Widada, J., Damayanti, E., & Dwi Wahyuningsih, T. (2020). Antiplasmodial activity of the low molecular weight compounds from Streptomyces sp. GMR22. Indonesian Journal of Pharmacy, 31(4), 273-280. https://www.swissadme.ch
Saigal, Irfan, M., Khan, P., Abid, M., & Khan, M. M. (2019). Design, synthesis, and biological evaluation of novel fused Spiro-4 H-pyran derivatives as bacterial biofilm disruptor. ACS Omega, 4(16), 16794–16807. https://doi.org/10.1021/acsomega.9b01571
Saito, H. E., Harp, J. R., & Fozo, E. M. (2014). Incorporation of exogenous fatty acids protects Enterococcus faecalis from membrane-damaging agents. Applied and Environmental Microbiology, 80(20), 6527–6538. https://doi.org/10.1128/AEM.02044-14
Seguel, N., Quezada-Aguiluz, M., González-Rocha, G., Bello-Toledo, H., & Sánchez-Sanhueza, G. (2020). Antibiotic resistance of Enterococcus faecalis from persistent endodontic infections. International Journal of. Odontostomatology, 14(3). 448-456.
Seipke, R. F. (2015). Strain-level diversity of secondary metabolism in Streptomyces albus. PLoS ONE, 10(1). e0116457. https://doi.org/10.1371/journal.pone.0116457
Senerovic, L., Opsenica, D., Moric, I., Aleksic, I., Spasić, M., & Vasiljevic, B. (2020). Quinolines and quinolones as antibacterial, antifungal, anti-virulence, antiviral and anti-parasitic agents. Advances in experimental medicine and biology, 1282, 37–69. https://doi.org/10.1007/5584_2019_428
Setiawati, S., & Yusan, R. T. (2022). Actinomycetes as a source of potential antimicrobial and antibiofilm agents. Medical and Health Journal, 1(2), 50. https://doi.org/10.20884/1.mhj.2022.1.2.5831
She, P., Wang, Y., Li, Y., Zhou, L., Li, S., Zeng, X., Liu, Y., Xu, L., & Wu, Y. (2021). Drug repurposing: in vitro and in vivo antimicrobial and antibiofilm effects of bithionol against Enterococcus faecalis and Enterococcus faecium. Frontiers in Microbiology, 12. 579806. https://doi.org/10.3389/fmicb.2021.579806
Sottorff, I., Wiese, J., Lipfert, M., Preußke, N., Sönnichsen, F. D., & Imhoff, J. F. (2019). Different secondary metabolite profiles of phylogenetically almost identical Streptomyces griseus strains originating from geographically remote locations. Microorganisms, 7(6), 166. https://doi.org/10.3390/microorganisms7060166
Stenz, L., François, P., Fischer, A., Huyghe, A., Tangomo, M., Hernandez, D., Cassat, J., Linder, P., & Schrenzel, J. (2008). Impact of oleic acid (cis-9-octadecenoic acid) on bacterial viability and biofilm production in Staphylococcus aureus. FEMS Microbiology Letters, 287(2), 149–155. https://doi.org/10.1111/j.1574-6968.2008.01316.x
Stuart, C., Schwartz, S., Beeson, T., & Owatz, C. (2006). Enterococcus faecalis: Its role in root canal treatment failure and current concepts in retreatment. Journal of Endodontics, 32(2), 93–98. https://doi.org/10.1016/j.joen.2005.10.049
Su, S., Yin, P., Li, J., Chen, G., Wang, Y., Qu, D., Li, Z., Xue, X., Luo, X., & Li, M. (2020). In vitro and in vivo anti-biofilm activity of pyran derivative against Staphylococcus aureus and Pseudomonas aeruginosa. Journal of Infection and Public Health, 13(5), 791–799. https://doi.org/10.1016/j.jiph.2019.10.010
Suhartono, S., Soraya, C., & Shabira, P. (2023). Antibiofilm activity of neem leaf (Azadirachta indica A. Juss) ethanolic extracts against Enterococcus faecalis in vitro. Dental Journal, 56(2), 98–103. https://doi.org/10.20473/J.DJMKG.V56.I2.P98-103
Wang, Q. Q., Zhang, C. F., Chu, C. H., & Zhu, X. F. (2012). Prevalence of Enterococcus faecalis in saliva and filled root canals of teeth associated with apical periodontitis. International Journal of Oral Science, 4(1), 19–23. https://doi.org/10.1038/ijos.2012.17
Waturangi, D. E., Rahayu, B. S., Lalu, K. Y., Michael, & Mulyono, N. (2016). Characterization of bioactive compound from Actinomycetes for antibiofilm activity against Gram-negative and Gram-positive bacteria. Malaysian Journal of Microbiology, 12(4), 291–299. https://doi.org/10.21161/mjm.80915
Windaryanti, D., Gabriel, C. S., Hidayat, I. W., Zainuddin, A., Dharsono, H. D. A., Satari, M. H., & Kurnia, D. (2022). The potential of 24-propylcholestrol as antibacterial oral bacteria of Enterococcus faecalis ATCC 29212 and inhibitor biofilms formation: in vitro and in silico study. Advances and Applications in Bioinformatics and Chemistry, 15, 99–111. https://doi.org/10.2147/AABC.S372337
Wong, J., Manoil, D., Näsman, P., Belibasakis, G. N., & Neelakantan, P. (2021). Microbiological aspects of root canal infections and disinfection strategies: an update review on the current knowledge and challenges. Frontiers in Oral Health, 2, 672887. https://doi.org/10.3389/froh.2021.672887
Xie, T. T., Zeng, H., Ren, X. P., Wang, N., Chen, Z. J., Zhang, Y., & Chen, W. (2019). Antibiofilm activity of three Actinomycete strains against Staphylococcus epidermidis. Letters in applied microbiology, 68(1), 73–80. https://doi.org/10.1111/lam.13087
Ye, L., Cao, L., Song, W., Yang, C., Tang, Q., & Yuan, Z. (2023). Interaction between apical periodontitis and systemic disease (Review). International Journal of Molecular Medicine, 52(1), 60. https://doi.org/10.3892/ijmm.2023.5263
Yuyama, K. T., Rohde, M., Molinari, G., Stadler, M., & Abraham, W. R. (2020). Unsaturated fatty acids control biofilm formation of Staphylococcus aureus and other Gram-positive bacteria. Antibiotics, 9(11), 1–11. https://doi.org/10.3390/antibiotics9110788
Zeng, X., She, P., Zhou, L., Li, S., Hussain, Z., Chen, L., & Wu, Y. (2021). Drug repurposing: Antimicrobial and antibiofilm effects of penfluridol against Enterococcus faecalis. MicrobiologyOpen, 10(1), e1148. https://doi.org/10.1002/mbo3.1148
Zoletti, G. O., Pereira, E. M., Schuenck, R. P., Teixeira, L. M., Siqueira, J. F., & dos Santos, K. R. N. (2011). Characterization of virulence factors and clonal diversity of Enterococcus faecalis isolates from treated dental root canals. Research in Microbiology, 162(2), 151–158. https://doi.org/10.1016/j.resmic.2010.09.018
Published
2025-06-16
How to Cite
Susilowati, H. (2025). The Potency of Soil Actinomycetes Extracts as Antibiofilm Agents against Enterococcus faecalis . Indonesian Journal of Pharmacy. https://doi.org/10.22146/ijp.13850
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Section
Research Article
