Skip to main content
SpringerLink
Log in

Ziziphus spina-christi (L.) Willd. Leaves Extract Affecting agr Quorum Sensing System in Staphylococcus aureus

  • Research Article-Biological Sciences
  • Published:
Arabian Journal for Science and Engineering Aims and scope Submit manuscript

Abstract

Ziziphus spina-christi L. (Sider) is a longstanding Arabian medicinal herb. The present study aimed to explore whether Ziziphus spina-christi leaves extract (ZSCLE) affects agr quorum sensing (QS) system and the phenotypic blood hemolytic activity regulated by this system in Staphylococcus aureus. The luciferase is encoded by plasmid pSB2035 in the reporter strain 8325–4, which is promoted by the agr P3 promoter. The result indicated that the total extract of (ZSCL) is effective against agr QS system in the reporter strain, where it reduces the lux gene expression up to 80.41% at a concentration of 0.25 mg/mL of total extract. Also, the hemolytic activity was reduced up to 98.9% by comparing with positive control by total extract. Successive extracts: hexane, diethyl ether, chloroform, ethyl acetate, and methanol were performed. The result revealed that the diethyl ether fraction was the greatest one that inhibited the production of both agr locus and the phenotypic hemolysin protein of S. aureus. Accordingly, phytochemical analysis in this total extract was performed and showed a high number of flavonoids and other compounds. FT-IR analysis of the most active fraction showed Monoelaidin as the main component of this fraction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

All authors declare that the data supporting the findings of this study are available within the article.

References

  1. Hossain, A.; Habibullah-Al-Mamun, M.; Nagano, I.; Masunaga, S.; Kitazawa, D.; Matsuda, H.: Antibiotics, antibiotic-resistant bacteria, and resistance genes in aquaculture: risks, current concern, and future thinking. Environ. Sci. Pollut. Res. 29, 1–22 (2022)

    Article  Google Scholar 

  2. Elfaky, M.A.; Abdel-Hamid, M.I.; Khalifa, E.; Alshareef, W.A.; Mosbah, R.A.; Elazab, S.T., et al.: Innovative next-generation therapies in combating multi-drug-resistant and multi-virulent Escherichia coli isolates: insights from in vitro, in vivo, and molecular docking studies. Appl. Microbiol. Biotechnol. 106, 1691–1703 (2022)

    Article  Google Scholar 

  3. Nassar, O.; Desouky, S.E.; El-Sherbiny, G.M.; Abu-Elghait, M.: Correlation between phenotypic virulence traits and antibiotic resistance in Pseudomonas aeruginosa clinical isolates. Microb. Pathog. 162, 105339 (2022)

    Article  Google Scholar 

  4. Yousef, A.; Abu-Elghait, M.; Barghoth, M.G.; Elazzazy, A.M.; Desouky, S.E.: Fighting multidrug-resistant Enterococcus faecalis via interfering with virulence factors using green synthesized nanoparticles. Microb. Pathog. 173, 105842 (2022)

    Article  Google Scholar 

  5. Johnson, D.I.: Bacterial virulence factors, p. 1–3. Bacterial pathogens and their virulence factors. Springer (2018)

    Book  Google Scholar 

  6. JoGdM, P.; Fernandes, L.S.; dos Santos, R.V.; Tasic, L.; Fill, T.P.: Virulence factors in the phytopathogen–host interactions: an overview. J. Agric. Food Chem. 68, 7555–7570 (2020)

    Article  Google Scholar 

  7. Rasko, D.A.; Sperandio, V.: Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9, 117–128 (2010)

    Article  Google Scholar 

  8. Dickey, S.W.; Cheung, G.Y.; Otto, M.: Different drugs for bad bugs: antivirulence strategies in the age of antibiotic resistance. Nat. Rev. Drug Discov. 16, 457–471 (2017)

    Article  Google Scholar 

  9. Escaich, S.: Antivirulence as a new antibacterial approach for chemotherapy. Curr. Opin. Chem. Biol. 12, 400–408 (2008)

    Article  Google Scholar 

  10. Loss, G.; Simões, P.M.; Valour, F.; Cortês, M.F.; Gonzaga, L.; Bergot, M., et al.: Staphylococcus aureus small colony variants (SCVs): news from a chronic prosthetic joint infection. Front. Cell. Infect. Microbiol. 9, 363 (2019)

    Article  Google Scholar 

  11. Tong, S.Y.; Davis, J.S.; Eichenberger, E.; Holland, T.L.; Fowler, V.G., Jr.: Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28, 603–661 (2015)

    Article  Google Scholar 

  12. El-gamal, M.S.; Desouky, S.E.; Hassan, S.E.; Elghait, M.A.: Phenotypic and biochemical characterization of specific virulence determinants regulated by agr quorum sensing system in Staphylococcus aureus. Al Azhar Bull Sci. 9, 217–226 (2017)

    Google Scholar 

  13. Chatterjee, A.; Rai, S.; Guddattu, V.; Mukhopadhyay, C.; Saravu, K.: Is methicillin-resistant Staphylococcus Aureus infection associated with higher mortality and morbidity in hospitalized patients? A cohort study of 551 patients from South Western India. Risk Manage. Healthcare Policy. 11, 243 (2018)

    Article  Google Scholar 

  14. Striednig, B.; Hilbi, H.: Bacterial quorum sensing and phenotypic heterogeneity: how the collective shapes the individual. Trends Microbiol. 30, 379–389 (2022)

    Article  Google Scholar 

  15. Ganesh, P.S.; Veena, K.; Senthil, R.; Iswamy, K.; Ponmalar, E.M.; Mariappan, V., et al.: Biofilm-associated Agr and Sar Quorum sensing systems of Staphylococcus aureus are Inhibited by 3-hydroxybenzoic acid derived from Illicium verum. ACS Omega 7, 14653–14665 (2022)

    Article  Google Scholar 

  16. Chevalier, C.; Boisset, S.; Romilly, C.; Masquida, B.; Fechter, P.; Geissmann, T., et al.: Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation. PLoS Pathog. 6, e1000809 (2010)

    Article  Google Scholar 

  17. Tam, K.; Torres, V.J.: Staphylococcus aureus secreted toxins and extracellular enzymes. Microbiol. Spectr. 7, 16 (2019)

    Article  Google Scholar 

  18. Okba, M.M.; Baki, P.M.A.; Abu-Elghait, M.; Shehabeldine, A.M.; El-Sherei, M.M.; Khaleel, A.E., et al.: UPLC-ESI-MS/MS profiling of the underground parts of common Iris species in relation to their anti-virulence activities against Staphylococcus aureus. J. Ethnopharmacol. 282, 114658 (2022)

    Article  Google Scholar 

  19. Desouky, S.E.; Abu-Elghait, M.; Fayed, E.A.; Selim, S.; Yousuf, B.; Igarashi, Y., et al.: Secondary metabolites of actinomycetales as potent quorum sensing inhibitors targeting gram-positive pathogens: in vitro and in silico study. Metabolites 12, 246 (2022)

    Article  Google Scholar 

  20. Hamed, A.; Abdel-Razek, A.S.; Araby, M.; Abu-Elghait, M.; El-Hosari, D.G.; Frese, M., et al.: Meleagrin from marine fungus Emericella dentata Nq45: crystal structure and diverse biological activity studies. Nat. Prod. Res. 35, 3830–3838 (2021)

    Article  Google Scholar 

  21. Tan, L.; Li, S.R.; Jiang, B.; Hu, X.M.; Li, S.: Therapeutic targeting of the Staphylococcus aureus accessory gene regulator (agr) system. Front. Microbiol. 9, 55 (2018)

    Article  Google Scholar 

  22. Chothani, D.L.; Vaghasiya, H.: A review on Balanites aegyptiaca Del (desert date): phytochemical constituents, traditional uses, and pharmacological activity. Pharmacogn. Rev. 5, 55 (2011)

    Article  Google Scholar 

  23. Sharma, V.; Sarkar, I.N.: Leveraging biodiversity knowledge for potential phyto-therapeutic applications. J. Am. Med. Inform. Assoc. 20, 668–679 (2013)

    Article  Google Scholar 

  24. CLSI. Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing. In: 20th informational supplement. CLSI document M100-S20. (2020).

  25. Okba, M.M.; El-Shiekh, R.A.; Abu-Elghait, M.; Sobeh, M.; Ashour, R.M.: HPLC-PDA-ESI-MS/MS Profiling and Anti-Biofilm Potential of Eucalyptus sideroxylon Flowers. Antibiotics. 10, 761 (2021)

    Article  Google Scholar 

  26. Azhagu, R.R.; Gomathi, M.; Prakasam, A.; Priya, K.; Narayanayyar, V.; Mahesh, P., et al.: Preliminary phyto-chemical analysis and biological activity of Hyptis suaveolens (L.)(Lamiaceae). Pharma Innov. 6, 1032 (2017)

    Google Scholar 

  27. Leela, C.; Shashank, B.; Suresh, D.: Phytochemical screening of secondary metabolites of Euphorbia Neriifolia Linn. Global J. Res. Med. Plants Indigenous Med. 2, 292 (2013)

    Google Scholar 

  28. Ren, X.; Guo, X.; Liu, C.; Jing, S.; Wang, T.; Wang, L., et al.: Natural flavone hispidulin protects mice from staphylococcus aureus pneumonia by inhibition of α-hemolysin production via targeting AgrAC. Microbiol. Res. 261, 127071 (2022)

    Article  Google Scholar 

  29. Cho, H.S.; Lee, J.-H.; Cho, M.H.; Lee, J.: Red wines and flavonoids diminish Staphylococcus aureus virulence with anti-biofilm and anti-hemolytic activities. Biofouling 31, 1–11 (2015)

    Article  Google Scholar 

  30. Soliman, M.K.; Salem, S.S.; Abu-Elghait, M.; Azab, M.S.: Biosynthesis of silver and gold nanoparticles and their efficacy towards antibacterial, antibiofilm, cytotoxicity, and antioxidant activities. Appl. Biochem. Biotechnol. 195, 1158–1183 (2023)

    Article  Google Scholar 

  31. Rahman, M.; Sarker, S.D.: Antimicrobial natural products. Annual Reports in Medicinal Chemistry, p. 77–113. Elsevier (2020)

    Google Scholar 

  32. Brannon, J.R.; Hadjifrangiskou, M.: The arsenal of pathogens and antivirulence therapeutic strategies for disarming them. Drug Des. Dev. Ther. 10, 1795 (2016)

    Google Scholar 

  33. Soliman, M.K.; Abu-Elghait, M.; Salem, S.S.; Azab, M.S.: Multifunctional properties of silver and gold nanoparticles synthesis by Fusarium pseudonygamai. Biomass Conver. Biorefinery 1–18 (2022)

  34. Ads, E.N.; Rajendrasozhan, S.; Hassan, S.I.; Sharawy, S.M.S.; Humaidi, J.R.: Phytochemical, antimicrobial and cytotoxic evaluation of Ziziphus spina-christi (L.) stem bark. Biomed. Res. 28, 6646–6653 (2017)

    Google Scholar 

  35. Ali, A.B.; Almagboul, A.Z.; Mohammed, O.M.: Antimicrobial activity of fruits, leaves, seeds and stems extracts of Ziziphus spina-christi. Arabian J. Med. Aromat. Plants 1, 94–107 (2015)

    Google Scholar 

  36. Motamedi, H.; Safary, A.; Maleki, S.; Seyyednejad, S.: Ziziphus spina-christi, a native plant from Khuzestan, Iran, as a potential source for discovery new antimicrobial agents. Asian J. Plant Sci. 8, 187 (2009)

    Article  Google Scholar 

  37. Dangoggo, S.; Hassan, L.; Sadiq, I.; Manga, S.: Phytochemical analysis and antibacterial screening of leaves of Diospyros mespiliformis and Ziziphus spina-christi. J. Chem. Eng. 1, 31–37 (2012)

    Google Scholar 

  38. Abalaka, M.; Mann, A.; Adeyemo, S.: Studies on in-vitro antioxidant and free radical scavenging potential and phytochemical screening of leaves of Ziziphus mauritiana L. and Ziziphus spinachristi L. compared with Ascorbic acid. J. Med. Genet. Genomics 3, 28–34 (2011)

    Google Scholar 

  39. Barbosa-Pereira, L.; Pocheville, A.; Angulo, I.; Paseiro-Losada, P.; Cruz, J.M.: Fractionation and purification of bioactive compounds obtained from a brewery waste stream. BioMed Res. Int. (2013). https://doi.org/10.1155/2013/408491

    Article  Google Scholar 

  40. Olchowik-Grabarek, E.; Sekowski, S.; Bitiucki, M.; Dobrzynska, I.; Shlyonsky, V.; Ionov, M., et al.: Inhibition of interaction between Staphylococcus aureus α-hemolysin and erythrocytes membrane by hydrolysable tannins: structure-related activity study. Sci. Rep. 10, 1–14 (2020)

    Article  Google Scholar 

Download references

Acknowledgements

This work was funded by the University of Jeddah, Jeddah, Saudi Arabia, under Grant No. (UJ-21-ICI-7). The authors, therefore, acknowledge with thanks the University of Jeddah technical and financial support.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, College of Science, University of Jeddah, Jeddah, Saudi Arabia

    Mohammed Y. Refai & Ahmed M. Elazzazy

  2. Department of Botany and Microbiology, Faculty of Science, Al-Azhar University, Cairo, 11884, Egypt

    Mohammed Abu-Elghait & Said Desouky

  3. Laboratory of Microbial Technology, Division of Systems Bioengineering, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School, Kyushu University, 744 Motooka, Nishi-Ku, Fukuoka, 819-0395, Japan

    Said Desouky & Jiro Nakayama

  4. Department of Biological Sciences, Faculty of Science, King Abdulaziz University, 21589, Jeddah, Saudi Arabia

    Mona O. I. Albureikan

Authors
  1. Mohammed Y. Refai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ahmed M. Elazzazy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammed Abu-Elghait
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Said Desouky
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mona O. I. Albureikan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiro Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MYR was involved in methodology, data recording, writing the manuscript, AME helped in methodology, chemical data analysis, writing the review, data reviewing, MA-E contributed to conceptualization, methodology, writing the first draft, data reviewing, SE helped in conceptualization, data reviewing, JN contributed to data reviewing, consultant.

Corresponding author

Correspondence to Ahmed M. Elazzazy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict interests.

Ethical Approval

This article does not contain any studies with human participants performed by any of the authors.

Consent to Participate

Authors understand that their participation is voluntary.

Consent to Publish

Authors give their consent for the publication of the article to be published in the Journal.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Refai, M.Y., Elazzazy, A.M., Abu-Elghait, M. et al. Ziziphus spina-christi (L.) Willd. Leaves Extract Affecting agr Quorum Sensing System in Staphylococcus aureus. Arab J Sci Eng 49, 97–105 (2024). https://doi.org/10.1007/s13369-023-08404-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13369-023-08404-5

Keywords

Search

Navigation