Abstract
This work aimed to evaluate the effects of 4 selected essential oils on planktonic cells and microbial biofilms of the Staphylococcus aureus strain (MRSA ATCC 33591). The antibacterial activities of the four essential oils Geranium (Pelargonium graveolens), PgEO, Tea Tree (Melaleuca alternifolia) MaEO, Lemon peel (Citrus limon) ClEO and Peppermint (Mentha piperita) MpEO had MICs ranging from 1.56 to 12.5 µl/ml. The evaluation of the antibiofilm activities of the 4 EOs revealed that they had antiadhesive activities against S. aureus MRSA biofilms; the activity reached 60% (the EO of MpEO peppermint at a concentration of 3.12 µl/ml), and the eradication activity was 80% (the EO of PgEO and MpEO at 3.12 µl/ml). The antibiofilm activity of S. aureus has been explained by the binding of several essential oil bioactive molecules to the SarA protein, the main target protein involved in biofilm formation. The synthesis of the virulence factor staphyloxanthin by S. aureus MRSA ATCC 33591 was significantly inhibited in the presence of PgEO at a concentration of MIC/2. This inhibition was explained by the binding of the main PgEO molecules (β-citronellol and geraniol) to the CrTM protein involved in the staphyloxanthin synthesis pathway. There is evidence that these essential oils could be used as potential anti-virulents to control Staphylococcus biofilm formation.
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Refrences
Williams-Nguyen J, Sallach JB, Bartelt-Hunt S et al (2016) Antibiotics and Antibiotic Resistance in Agroecosystems: state of the Science. J Environ Qual 45:394–406. https://doi.org/10.2134/jeq2015.07.0336
Salam MA, Al-Amin MY, Salam MT et al (2023) Antimicrobial Resistance: a growing serious threat for Global Public Health. Healthc (Basel) 11(1946). https://doi.org/10.3390/healthcare11131946
Neville N, Jia Z (2019) Approaches to the structure-based design of Antivirulence drugs: therapeutics for the post-antibiotic era. https://doi.org/10.3390/molecules24030378. Molecules
Murugaiyan J, Kumar PA, Rao GS et al (2022) Progress in alternative strategies to Combat Antimicrobial Resistance: focus on antibiotics. Antibiot (Basel) 11:200. https://doi.org/10.3390/antibiotics11020200
Buroni S, Chiarelli LR (2020) Antivirulence compounds: a future direction to overcome antibiotic resistance? Future Microbiol 15:299–301. https://doi.org/10.2217/fmb-2019-0294
Ma R, K G MM (2021) Microbial biofilm: formation, architecture, antibiotic resistance, and control strategies. Brazilian J Microbiology: [publication Brazilian Soc Microbiology] 52. https://doi.org/10.1007/s42770-021-00624-x
Singh A, Amod A, Pandey P et al (2022) Bacterial biofilm infections, their resistance to antibiotics therapy and current treatment strategies. Biomedical Mater (Bristol England) 17. https://doi.org/10.1088/1748-605X/ac50f6
Nikolic P, Mudgil P (2023) The cell wall, cell membrane and virulence factors of Staphylococcus aureus and their role in Antibiotic Resistance. Microorganisms 11:259. https://doi.org/10.3390/microorganisms11020259
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199. https://doi.org/10.1146/annurev.micro.55.1.165
Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
Beenken KE, Blevins JS, Smeltzer MS (2003) Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect Immun 71:4206–4211. https://doi.org/10.1128/IAI.71.7.4206-4211.2003
Yang Y, Wang H, Zhou H et al (2020) Protective effect of the Golden Staphyloxanthin Biosynthesis Pathway on Staphylococcus aureus under Cold Atmospheric plasma treatment. Appl Environ Microbiol 86:e01998–e01919. https://doi.org/10.1128/AEM.01998-19
Xue L, Chen YY, Yan Z et al (2019) Staphyloxanthin: a potential target for antivirulence therapy. Infect Drug Resist 12:2151–2160. https://doi.org/10.2147/IDR.S193649
Martínez A, Stashenko EE, Sáez RT et al (2023) Effect of essential oil from Lippia origanoides on the Transcriptional expression of genes related to Quorum Sensing, Biofilm formation, and virulence of Escherichia coli and Staphylococcus aureus. Antibiot (Basel) 12:845. https://doi.org/10.3390/antibiotics12050845
Boukhris M, Bouaziz M, Feki I et al (2012) Hypoglycemic and antioxidant effects of leaf essential oil of Pelargonium graveolens L’Hér. In alloxan induced diabetic rats. Lipids Health Dis 11:81. https://doi.org/10.1186/1476-511X-11-81
Bauer J, Siala W, Tulkens PM, Van Bambeke F (2013) A combined pharmacodynamic quantitative and qualitative model reveals the potent activity of daptomycin and delafloxacin against Staphylococcus aureus biofilms. Antimicrob Agents Chemother 57:2726–2737. https://doi.org/10.1128/AAC.00181-13
CLSI Clinical and Laboratory Standards Institute (CLSI) (2020) Performance Standards for Antimicrobial Susceptibility Testing. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute. https://www.nih.org.pk/wp-content/uploads/2021/02/CLSI-2020.pdf. Accessed 22 Apr 2024
Jardak M, Mnif S, Ben Ayed R et al (2021) Chemical composition, antibiofilm activities of Tunisian spices essential oils and combinatorial effect against Staphylococcus epidermidis biofilm. LWT 140:110691. https://doi.org/10.1016/j.lwt.2020.110691
Abdelli F, Jardak M, Elloumi J et al (2019) Antibacterial, anti-adherent and cytotoxic activities of surfactin(s) from a lipolytic strain Bacillus safensis F4. Biodegradation 30:287–300. https://doi.org/10.1007/s10532-018-09865-4
Kavanaugh NL, Ribbeck K (2012) Selected antimicrobial essential oils eradicate Pseudomonas spp. and Staphylococcus aureus biofilms. Appl Environ Microbiol 78:4057–4061. https://doi.org/10.1128/AEM.07499-11
Selvaraj A, Valliammai A, Muthuramalingam P et al (2020) Carvacrol targets SarA and CrtM of Methicillin-Resistant Staphylococcus aureus to Mitigate Biofilm formation and Staphyloxanthin Synthesis: an in Vitro and in vivo Approach. ACS Omega 5:31100–31114. https://doi.org/10.1021/acsomega.0c04252
Ryt PGJD K (2017) Dehydrosqualene Desaturase as a Novel Target for Anti-virulence Therapy against Staphylococcus aureus. https://doi.org/10.1128/mBio.01224-17. mBio 8:
Senthil Kumar KJ, Gokila Vani M, Wang C-S et al (2020) Geranium and Lemon essential oils and their active compounds Downregulate angiotensin-converting enzyme 2 (ACE2), a SARS-CoV-2 spike receptor-binding domain, in epithelial cells. Plants (Basel) 9:770. https://doi.org/10.3390/plants9060770
Corona-Gómez L, Hernández-Andrade L, Mendoza-Elvira S et al (2022) In vitro antimicrobial effect of essential tea tree oil(Melaleuca alternifolia), thymol, and carvacrol on microorganisms isolated from cases of bovine clinical mastitis. Int J Vet Sci Med 10:72–79. https://doi.org/10.1080/23144599.2022.2123082
Ben Hsouna A, Ben Halima N, Smaoui S, Hamdi N (2017) Citrus lemon essential oil: chemical composition, antioxidant and antimicrobial activities with its preservative effect against Listeria monocytogenes inoculated in minced beef meat. Lipids Health Dis 16:146. https://doi.org/10.1186/s12944-017-0487-5
Marwa C, Fikribenbrahim K, OU-yahia D, Farah A (2017) African peppermint (Mentha Piperita) from Morocco: Chemical composition and antimicrobial properties of essential oil. J Adv Pharm Tech Res 8. https://doi.org/10.4103/japtr.JAPTR_11_17
Ben ElHadj Ali I, Tajini F, Boulila A et al (2020) Bioactive compounds from Tunisian Pelargonium graveolens (L’Hér.) Essential oils and extracts: α-amylase and acethylcholinesterase inhibitory and antioxidant, antibacterial and phytotoxic activities. Ind Crops Prod 158:112951. https://doi.org/10.1016/j.indcrop.2020.112951
Cáceres M, Hidalgo W, Stashenko E et al (2020) Essential Oils of Aromatic Plants with Antibacterial, Anti-biofilm and Anti-quorum sensing activities against pathogenic Bacteria. Antibiot (Basel) 9:147. https://doi.org/10.3390/antibiotics9040147
Jardak M, Elloumi-Mseddi J, Aifa S, Mnif S (2017) Chemical composition, anti-biofilm activity and potential cytotoxic effect on cancer cells of Rosmarinus officinalis L. essential oil from Tunisia. Lipids Health Dis 16:190. https://doi.org/10.1186/s12944-017-0580-9
Balamurugan P, Praveen Krishna V, Bharath D et al (2017) Staphylococcus aureus Quorum Regulator SarA targeted compound, 2-[(Methylamino)methyl]phenol inhibits Biofilm and Down-regulates virulence genes. Front Microbiol 8:1290. https://doi.org/10.3389/fmicb.2017.01290
Liu C-I, Liu GY, Song Y et al (2008) A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus Virulence. Science 319:1391–1394. https://doi.org/10.1126/science.1153018
Zapotoczna M, McCarthy H, Rudkin JK et al (2015) An essential role for Coagulase in Staphylococcus aureus Biofilm Development reveals new therapeutic possibilities for device-related infections. J Infect Dis 212:1883–1893. https://doi.org/10.1093/infdis/jiv319
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This work was supported by the Ministry of Higher Education and Scientific Research of Tunisia (LR15CBS07 budget).
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Elghali, F., Ibrahim, I., Guesmi, M. et al. Unveiling the impact of selected essential oils on MRSA strain ATCC 33591: antibacterial efficiency, biofilm disruption, and staphyloxanthin inhibition. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01374-2
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DOI: https://doi.org/10.1007/s42770-024-01374-2