Phytochemical composition and antimicrobial, and anti-quorum sensing activities of Punica granatum L. methanolic extract
,
Abstract
Background and Objectives: In this work, our aims were to investigate the antimicrobial resistance, and anti-quorum sensing activities of Punica granatum L. methanolic extract.
Materials and Methods: Antibacterial and antifungal activities were performed against thirteen bacteria and five fungal pathogens. Ultra-high performance liquid chromatography was used to identify the polyphenolic extract. The inhibition of pyocyanin production, proteolytic and elastolytic activity and swarming motility in Pseudomonas aeruginosa PAO1 test strain were estimated.
Results: The methanolic extract from P. granatum L. was dominated by chlorogenic acid (34.028 mg/g), rutin (26.05 mg/g), epicatechin (12.207 mg/g), gallic acid (11.157 mg/g), and caffeic acid 9.768 mg/g). Results showed antibacterial activities against almost all tested microorganisms with mean diameter of growth inhibition zone ranging from 6 ± 0 to 30 ± 0 mm for Candida species and from 6 ± 0 to 22.66 ± 0.57 for bacterial strains. The lowest minimal inhibitory concentrations were recorded for Listeria monocytogenes ATCC 19115 and Salmonella enterica CECT 529 (0.14 mg/ml, respectively). The anti-quorum sensing activity of methanolic extract against P. aeruginosa showed a significant inhibition of swarming motility and an attenuation in virulence factors like pyocyanin production at low concentrations.
Conclusion: The obtained results indicates that P. granatum L. extracts is a rich source of phenolic compounds and highlighted the possibilities uses of pomegranate to attenuate the expression of quorum sensing controlled factors in P. aeruginosa PAO1 strain.
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3. Ali BH, Wabel NA, Blunden G. Phytochemical, pharmacological and toxicological aspects of Hibiscus sabdariffa L.: a review. Phytother Res 2005 ; 19: 369-375.
4. Egharevba RKA, Ikhatua MI. Ethno-medical uses of plants in the treatment of various skin diseases in Ovia North East, Edo State, Nigeria. Res J Agric Biol Sci 2008; 4: 58-64.
5. Gangrade H, Mishra SH, Kaushal R. Antimicrobial activity of the oil and unsaponifiable matter of red hibiscus. Indian Drugs 1979; 16: 147-148.
6. Abdallah EM. Antibacterial activity of Hibiscus sabdariffa L, calyces against hospital isolates of multidrug resistant Acinetobacter baumannii. J Acute Dis 2016; 5: 512-516.
7. Longtin R. The Pomegranate: Nature’s Power Fruit?’. J Natl Cancer Inst 2003; 95: 346-348.
8. Howell AB, D’Souza DH. The pomegranate: effects on bacteria and viruses that influence human health. Evid Based Complement Alternat Med 2013; 2013: 606212.
9. Al-Zoreky NS. Antimicrobial activity of pomegranate (Punica granatum L.) fruit peels. Int J Food Microbiol 2009; 134: 244-248.
10. Ben Nasr C, Ayed N, Metche M. Quantitative determination of the polyphenolic content of pomegranate peel. Z Lebensm Unters Forsch 1996; 203: 374-378.
11. Hora JJ, Maydew ER, Lansky EP, Dwivedi C. Chemopreventive effects of pomegranate seed oil on skin tumor development in CD1 mice. J Med Food 2003; 6: 157-161.
12. Mehta R, Lansky EP. Breast cancer chemopreventive properties of pomegranate Punica granatum fruit extracts in a mouse mammary organ culture. Eur J Cancer Prev 2004; 13: 345-348.
13. Adams LS, Seeram NP, Aggarwal BB, Takada Y, Sand D, Heber D. Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells. J Agric Food Chem 2006; 54: 980-985.
14. Singh R, Singh MK, Chandra LR. In vitro antioxidant and free radical scavenging activity of Macrotyloma uniflorum Gahat dal from Kumauni region. Int J Fundam Appl Sci 2012; 1: 7-10.
15. Schubert A, Pereira DF, Zanin FF, Alves SH, Beck RCR, Athayde ML. Comparison of antioxidant activities and total polyphenolic and methylxanthine contents between the unripe fruit and leaves of Ilex paraguariensis A. St Hil. Pharmazie 2007; 62: 876-880.
16. Gil MI, Tomás-Barberán FA, Hess-Pierce B, Holcroft DM, Kader AA. Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing. J Agric Food Chem 2000; 48: 4581-4589.
17. Aviram M, Fuhrman B. Polyphenolic flavonoids inhibit macrophage-mediated oxidation of LDL and attenuate atherogenesis. Atherosclerosis 1998; 137 Suppl: S45-50.
18. Chidambara Murthy KN, Jayaprakasha GK, Singh RP. Studies on antioxidant activity of pomegranate (Punica granatum) peel extract using in vivo models. J Agric Food Chem 2002; 50: 4791-4795.
19. Middha SK, Usha T, Pande V. HPLC evaluation of phenolic profile, nutritive content, and antioxidant capacity of extracts obtained from Punica granatum fruit peel. Adv Pharmacol Sci 2013; 2013: 296236.
20. Natić MM, Dabić DČ, Papetti A, Fotirić Akšić MM, Ognjanov V, Ljubojević M, et al. Analysis and characterisation of phytochemicals in mulberry (Morus alba L.) fruits grown in Vojvodina, north Serbia. Food Chem 2015; 171: 128-136.
21. Snoussi M, Noumi E, Cheriaa J, Usai D, Sechi LA, Zanetti S, et al. Adhesive properties of environmental Vibrio alginolyticus strains to biotic and abiotic surfaces. New Microbiol 2008; 31: 489-500.
22. Hamoud R, Zimmermann S, Reichling J, Wink M. Synergistic interaction in two-drug and three-drug combinations (thymol, EDTA and vancomycin) against multidrug resistant bacteria including E. coli. Phytomedicine 2014; 21: 443-447.
23. Clemmer KM, Bonomo RA, Rather PN. Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology (Reading) 2011; 157: 2534-2544.
24. Vasavi HS, Arun AB, Rekha PD. Anti-quorum sensing activity of Psidium guajava L. flavonoids against Chromobacterium violaceum and Pseudomonas aeruginosa PAO1. Microbiol Immunol 2014; 58: 286-293.
25. Dong YH, Zhang XF, Soo HM, Greenberg EP, Zhang LH. The two-component response regulator PprB modulates quorum-sensing signal production and global gene expression in Pseudomonas aeruginosa. Mol Microbiol 2005; 56: 1287-1301.
26. Snoussi M, Trabelsi N, Dehmeni A, Benzekri R, Bouslama L, Hajlaoui B, et al. Phytochemical analysis antimicrobial and antioxidant activities of Allium roseum Var. odoratissimum Desf. Coss extracts. Ind Crops Prod 2016; 89: 533-542.
27. Joshi C, Patel P, Kothari V. Anti-infective potential of hydroalcoholic extract of Punica granatum peel against gram-negative bacterial pathogens. F1000Res 2019; 8: 58-70.
28. da Silva PM, de Moura MC, Gomes FS, da Silva Trentin D, Silva de Oliveira AP, de Mello GSV, et al. PgTeL the lectin found in Punica granatum juice, is an antifungal agent against Candida albicans and Candida krusei. Int J Biol Macromol 2018; 108: 391-400.
29. Elmanama AA, Al-Reefi MR. Antimicrobial, anti-biofilm, anti-quorum sensing, antifungal and synergistic effects of some medicinal plants extracts. IUG J Nat Stud 2017; 25: 198-207.
30. Kalemba D, Kunicka A. Antibacterial and antifungal properties of essential oils. Curr Med Chem 2003; 10: 813-829.
31. Sindi HA, Marshall LJ, Morgan MR. Comparative chemical and biochemical analysis of extracts of Hibiscus sabdariffa. Food Chem 2014; 164: 23-29.
32. Endo EH, Cortez DA, Ueda-Nakamura T, Nakamura CV, Dias Filho BP. Potent antifungal activity of extracts and pure compound isolated from pomegranate peels and synergism with fluconazole against Candida albicans. Res Microbiol 2010; 161: 534-540.33. Dey D, Debnath S, Hazra S, Ghosh S, Ray R, Hazra B. Pomegranate pericarp extract enhances
the antibacterial activity of ciprofloxacin against extended-spectrum β-lactamase (ESBL) and metallo-β-lactamase (MBL) producing Gram-negative bacilli. Food Chem Toxicol 2012; 50: 4302-4309.34. Zhou JW, Jia AQ, Jiang H, Li PL, Chen H,
Tan XJ, et al. 1-(4-Amino-2-hydroxyphenyl) ethanone from Phomopsis liquidambari showed quorum sensing inhibitory activity against Pseudomonas aeruginosa. Appl Microbiol Biotechnol 2021; 105: 341-352.
35. Li G, Yan C, Xu Y, Feng Y, Wu Q, Lv X, et al. Punicalagin inhibits Salmonella virulence factors and has anti-quorum-sensing potential. Appl Environ Microbiol 2014; 80: 6204-6211.
36. Mahadwar G, Chauhan KR, Bhagavathy GV, Murphy C, Smith AD, Bhagwat AA. Swarm motility of Salmonella enterica serovar Typhimurium is inhibited by compounds from fruit peel extracts. Lett Appl Microbiol 2015; 60: 334-
340.37. Yang Q, Wang L, Gao J, Liu X, Feng Y, Wu Q, et al. Tannin-Rich fraction from pomegranate rind inhibits quorum sensing in Chromobacterium violaceum and biofilm formation in Escherichia coli. Foodborne Pathog Dis 2016; 13: 28-35.
38. Khemakhem M, Zarroug Y, Jabou K, Selmi S, Bouzouita N. Physicochemical characterization of oil, antioxidant potential, and phenolic profile of seeds isolated from Tunisian pomegranate Punica granatum L. cultivars. J Food Sci 2021; 86: 852-859.
2. Farombi EO, Fakoya A. Free radical scavenging and antigenotoxic activities of natural phenolic compounds in dried flowers of Hibiscus sabdariffa L. Mol Nutr Food Res 2005; 49: 1120-1128.
3. Ali BH, Wabel NA, Blunden G. Phytochemical, pharmacological and toxicological aspects of Hibiscus sabdariffa L.: a review. Phytother Res 2005 ; 19: 369-375.
4. Egharevba RKA, Ikhatua MI. Ethno-medical uses of plants in the treatment of various skin diseases in Ovia North East, Edo State, Nigeria. Res J Agric Biol Sci 2008; 4: 58-64.
5. Gangrade H, Mishra SH, Kaushal R. Antimicrobial activity of the oil and unsaponifiable matter of red hibiscus. Indian Drugs 1979; 16: 147-148.
6. Abdallah EM. Antibacterial activity of Hibiscus sabdariffa L, calyces against hospital isolates of multidrug resistant Acinetobacter baumannii. J Acute Dis 2016; 5: 512-516.
7. Longtin R. The Pomegranate: Nature’s Power Fruit?’. J Natl Cancer Inst 2003; 95: 346-348.
8. Howell AB, D’Souza DH. The pomegranate: effects on bacteria and viruses that influence human health. Evid Based Complement Alternat Med 2013; 2013: 606212.
9. Al-Zoreky NS. Antimicrobial activity of pomegranate (Punica granatum L.) fruit peels. Int J Food Microbiol 2009; 134: 244-248.
10. Ben Nasr C, Ayed N, Metche M. Quantitative determination of the polyphenolic content of pomegranate peel. Z Lebensm Unters Forsch 1996; 203: 374-378.
11. Hora JJ, Maydew ER, Lansky EP, Dwivedi C. Chemopreventive effects of pomegranate seed oil on skin tumor development in CD1 mice. J Med Food 2003; 6: 157-161.
12. Mehta R, Lansky EP. Breast cancer chemopreventive properties of pomegranate Punica granatum fruit extracts in a mouse mammary organ culture. Eur J Cancer Prev 2004; 13: 345-348.
13. Adams LS, Seeram NP, Aggarwal BB, Takada Y, Sand D, Heber D. Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells. J Agric Food Chem 2006; 54: 980-985.
14. Singh R, Singh MK, Chandra LR. In vitro antioxidant and free radical scavenging activity of Macrotyloma uniflorum Gahat dal from Kumauni region. Int J Fundam Appl Sci 2012; 1: 7-10.
15. Schubert A, Pereira DF, Zanin FF, Alves SH, Beck RCR, Athayde ML. Comparison of antioxidant activities and total polyphenolic and methylxanthine contents between the unripe fruit and leaves of Ilex paraguariensis A. St Hil. Pharmazie 2007; 62: 876-880.
16. Gil MI, Tomás-Barberán FA, Hess-Pierce B, Holcroft DM, Kader AA. Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing. J Agric Food Chem 2000; 48: 4581-4589.
17. Aviram M, Fuhrman B. Polyphenolic flavonoids inhibit macrophage-mediated oxidation of LDL and attenuate atherogenesis. Atherosclerosis 1998; 137 Suppl: S45-50.
18. Chidambara Murthy KN, Jayaprakasha GK, Singh RP. Studies on antioxidant activity of pomegranate (Punica granatum) peel extract using in vivo models. J Agric Food Chem 2002; 50: 4791-4795.
19. Middha SK, Usha T, Pande V. HPLC evaluation of phenolic profile, nutritive content, and antioxidant capacity of extracts obtained from Punica granatum fruit peel. Adv Pharmacol Sci 2013; 2013: 296236.
20. Natić MM, Dabić DČ, Papetti A, Fotirić Akšić MM, Ognjanov V, Ljubojević M, et al. Analysis and characterisation of phytochemicals in mulberry (Morus alba L.) fruits grown in Vojvodina, north Serbia. Food Chem 2015; 171: 128-136.
21. Snoussi M, Noumi E, Cheriaa J, Usai D, Sechi LA, Zanetti S, et al. Adhesive properties of environmental Vibrio alginolyticus strains to biotic and abiotic surfaces. New Microbiol 2008; 31: 489-500.
22. Hamoud R, Zimmermann S, Reichling J, Wink M. Synergistic interaction in two-drug and three-drug combinations (thymol, EDTA and vancomycin) against multidrug resistant bacteria including E. coli. Phytomedicine 2014; 21: 443-447.
23. Clemmer KM, Bonomo RA, Rather PN. Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology (Reading) 2011; 157: 2534-2544.
24. Vasavi HS, Arun AB, Rekha PD. Anti-quorum sensing activity of Psidium guajava L. flavonoids against Chromobacterium violaceum and Pseudomonas aeruginosa PAO1. Microbiol Immunol 2014; 58: 286-293.
25. Dong YH, Zhang XF, Soo HM, Greenberg EP, Zhang LH. The two-component response regulator PprB modulates quorum-sensing signal production and global gene expression in Pseudomonas aeruginosa. Mol Microbiol 2005; 56: 1287-1301.
26. Snoussi M, Trabelsi N, Dehmeni A, Benzekri R, Bouslama L, Hajlaoui B, et al. Phytochemical analysis antimicrobial and antioxidant activities of Allium roseum Var. odoratissimum Desf. Coss extracts. Ind Crops Prod 2016; 89: 533-542.
27. Joshi C, Patel P, Kothari V. Anti-infective potential of hydroalcoholic extract of Punica granatum peel against gram-negative bacterial pathogens. F1000Res 2019; 8: 58-70.
28. da Silva PM, de Moura MC, Gomes FS, da Silva Trentin D, Silva de Oliveira AP, de Mello GSV, et al. PgTeL the lectin found in Punica granatum juice, is an antifungal agent against Candida albicans and Candida krusei. Int J Biol Macromol 2018; 108: 391-400.
29. Elmanama AA, Al-Reefi MR. Antimicrobial, anti-biofilm, anti-quorum sensing, antifungal and synergistic effects of some medicinal plants extracts. IUG J Nat Stud 2017; 25: 198-207.
30. Kalemba D, Kunicka A. Antibacterial and antifungal properties of essential oils. Curr Med Chem 2003; 10: 813-829.
31. Sindi HA, Marshall LJ, Morgan MR. Comparative chemical and biochemical analysis of extracts of Hibiscus sabdariffa. Food Chem 2014; 164: 23-29.
32. Endo EH, Cortez DA, Ueda-Nakamura T, Nakamura CV, Dias Filho BP. Potent antifungal activity of extracts and pure compound isolated from pomegranate peels and synergism with fluconazole against Candida albicans. Res Microbiol 2010; 161: 534-540.33. Dey D, Debnath S, Hazra S, Ghosh S, Ray R, Hazra B. Pomegranate pericarp extract enhances
the antibacterial activity of ciprofloxacin against extended-spectrum β-lactamase (ESBL) and metallo-β-lactamase (MBL) producing Gram-negative bacilli. Food Chem Toxicol 2012; 50: 4302-4309.34. Zhou JW, Jia AQ, Jiang H, Li PL, Chen H,
Tan XJ, et al. 1-(4-Amino-2-hydroxyphenyl) ethanone from Phomopsis liquidambari showed quorum sensing inhibitory activity against Pseudomonas aeruginosa. Appl Microbiol Biotechnol 2021; 105: 341-352.
35. Li G, Yan C, Xu Y, Feng Y, Wu Q, Lv X, et al. Punicalagin inhibits Salmonella virulence factors and has anti-quorum-sensing potential. Appl Environ Microbiol 2014; 80: 6204-6211.
36. Mahadwar G, Chauhan KR, Bhagavathy GV, Murphy C, Smith AD, Bhagwat AA. Swarm motility of Salmonella enterica serovar Typhimurium is inhibited by compounds from fruit peel extracts. Lett Appl Microbiol 2015; 60: 334-
340.37. Yang Q, Wang L, Gao J, Liu X, Feng Y, Wu Q, et al. Tannin-Rich fraction from pomegranate rind inhibits quorum sensing in Chromobacterium violaceum and biofilm formation in Escherichia coli. Foodborne Pathog Dis 2016; 13: 28-35.
38. Khemakhem M, Zarroug Y, Jabou K, Selmi S, Bouzouita N. Physicochemical characterization of oil, antioxidant potential, and phenolic profile of seeds isolated from Tunisian pomegranate Punica granatum L. cultivars. J Food Sci 2021; 86: 852-859.
| Files | ||
| Issue | Vol 14 No 3 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i3.9778 | |
| Keywords | ||
| Punica granatum L; Antimicrobial activities; Pseudomonas aeruginosa PAO1; Swarming; Proteolytic activity; Elastolytic activity | ||
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How to Cite
1.
Hamrita B, Noumi E, Hafi F, Nazzaro F, Snoussi M. Phytochemical composition and antimicrobial, and anti-quorum sensing activities of Punica granatum L. methanolic extract. Iran J Microbiol. 2022;14(3):373-382.
