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Bioactivities and in silico study of Pergularia tomentosa L. phytochemicals as potent antimicrobial agents targeting type IIA topoisomerase, TyrRS, and Sap1 virulence proteins

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Abstract

Pergularia tomentosa L. (P. tomentosa) has been largely used in Tunisian folk medicine as remedies against skin diseases, asthma, and bronchitis. The main objectives of this study were to identify phytochemical compounds that have antioxidant and antimicrobial properties from the stem, leaves, and fruit crude methanolic extracts of P. tomentosa, and to search for tyrosyl-tRNA synthetase (TyrRS), topoisomerase type IIA, and Candidapepsin-1 (SAP1) enzyme inhibitors through molecular docking study. Phytochemical quantification revealed that fruit and leaves extracts displayed the highest total flavonoids (582 mg QE/g Ex; 219 mg QE/g Ex) and tannins content (375 mg TAE/g Ex; 216 mg TAE/g Ex), also exhibiting significant scavenging activity to decrease free radicals for ABTS, DPPH, β-carotene, and FRAP assay with IC50 values (> 1 mg/mL). Additionally, promising antimicrobial activities towards different organs have been observed against several bacteria and Candida strains. From the liquid chromatography-mass spectrometry (LC-MS) analysis, five polyphenolic compounds, namely digitoxigenin, digitonin glycoside and calactina in the leaves, kaempferol in the fruit, and calotropagenin in the stems, were identified. They were also analyzed for their drug likeliness, based on computational methods. Molecular docking study affirmed that the binding affinity of calactin and actodigin to the active site of TyrRS, topoisomerase type IIA, and SAP1 target virulence proteins was the highest among the examined dominant compounds. Therefore, this study indicated that P. tomentosa methanolic extracts displayed great potential to become a potent antimicrobial agent and might be a promising source for therapeutic and nutritional functions. These phytocompounds could be further promoted as a candidate for drug discovery and development.

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All data generated or analyzed during this study are included in this published article. Additional information will be available upon request.

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Acknowledgments

The authors would like to thank Dr. Hafedh Hajlaoui (Research Unit Valorization and Optimization of Resource Exploitation (UR16ES04), Faculty of Science and Technology of Sidi Bouzid, University of Kairouan, Campus University Agricultural City—Sidi Bouzid 9100, Tunisia), for collecting material samples.

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Authors and Affiliations

  1. Laboratory of Genetics, Biodiversity and Valorization of Bio-resources (LR11ES41), University of Monastir, Higher Institute of Biotechnology of Monastir, Avenue Tahar Haddad, BP74, 5000, Monastir, Tunisia

    Fatma Haddaji

  2. Nutraceutical & Food Chemical-Toxicological Analysis Laboratory, Department of Drug Sciences, University of Pavia, Viale Taramelli 12, 27100, Pavia, Italy

    Adele Papetti & Raffaella Colombo

  3. Department of Biology, College of Science, University of Ha’il, P.O. 2440, Hail, Saudi Arabia

    Emira Noumi, Mohd Adnan & Mejdi Snoussi

  4. Laboratory of Bioressources: Integrative Biology and Valorization, (LR14-ES06), University of Monastir, Higher Institute of Biotechnology of Monastir, Avenue Tahar Haddad, BP 74, 5000, Monastir, Tunisia

    Emira Noumi & Boulbaba Selmi

  5. Central Biotechnology Services, College of Biomedical and Life Sciences, Cardiff University, Cardiff, Wales, CF14 4XN, UK

    Sumukh Deshpande

  6. Faculty of Science and Arts in Baljurashi, Albaha University, P.O. Box 1988, Albaha, Saudi Arabia

    Kaïss Aouadi

  7. Faculty of Science of Monastir, Laboratory of Hetrocyclic Chemistry, Natural Products and Reactivity, Avenue of the Environment, University of Monastir, 5019, Monastir, Tunisia

    Kaïss Aouadi

  8. Faculty of Science of Sfax, Department of Chemistry, University of Sfax, B.P. 1171, 3000, Sfax, Tunisia

    Adel Kadri

  9. Department of Chemistry, College of Science, Qassim University, Buraidah, 51452, Saudi Arabia

    Adel Kadri

Authors
  1. Fatma Haddaji
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  2. Adele Papetti
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  3. Emira Noumi
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  7. Mohd Adnan
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  8. Adel Kadri
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  9. Boulbaba Selmi
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Contributions

Dr. Fatma Haddagi: performed experimental work related to plant extraction, antimicrobial activities testing, data analysis, and original draft writing. Prof. Adele Papetti and Prof. Rafaella Colombo: analyzed the phytochemical composition of the obtained extracts, helped in paper revision, and editing. Dr. Emira Noumi: experimental supervision and data collection and analysis. Dr. Sumukh Deshpande and Dr. Mohd Adnan: performed the computational study and helped in original draft writing. Dr. Kaiis Aouadi: performed ADMET prediction. Prof. Adel Kadri: analyzed all data obtained related to pharmacokinetic properties and toxicity prediction and helped in the final paper editing and revising. Prof. Boulbaba Selmi: Co-supervision. Dr. Mejdi Snoussi: designed the work, supervised the experimental work, helped in formal analysis, and original draft writing.

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Correspondence to Mejdi Snoussi.

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Responsible editor: Mohamed M. Abdel-Daim

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Haddaji, F., Papetti, A., Noumi, E. et al. Bioactivities and in silico study of Pergularia tomentosa L. phytochemicals as potent antimicrobial agents targeting type IIA topoisomerase, TyrRS, and Sap1 virulence proteins. Environ Sci Pollut Res 28, 25349–25367 (2021). https://doi.org/10.1007/s11356-020-11946-y

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