Antibacterial activity of Shallots (Allium xwakegi Araki.) cultivars in Palu Valley against Salmonella Typhi ATCC 27870 through in vitro and in silico evaluation
,
Abstract
Background and Objectives: Shallots, recognized for their minimal toxicity, cost-effectiveness, and widespread availability, are increasingly considered a viable source of biological activity. This study evaluates the antibacterial efficacy of a specific shallot cultivar from Palu Valley, Indonesia, against Salmonella typhi, the pathogen responsible for typhoid fever.
Materials and Methods: Utilizing thin-layer chromatography (TLC-bioautography) and gas chromatography-mass spectroscopy (GC-MS), the study identifies active compounds in shallot ethanol extract and employs molecular docking to assess interactions between receptors and ligands.
Results: Findings indicate significant antibacterial activity, with a notable inhibition zone diameter of 31.5 mm at spot Rf 0.28 in TLC bioautography and an optimum concentration of 2% yielding an average clear zone diameter of 28.27 mm in the agar diffusion test. GC-MS analysis reveals 41 compounds, predominantly dodecanoic acid and 1,2,3-propanetriyl ester. Additionally, molecular docking reveals the lowest binding affinity (-7.3 kcal/mol) for Ergost-8-En-3-Ol, 14-Methyl-, (3.Beta,5.Alpha.) against DNA gyrase.
Conclusion: This study confirms Palu Valley shallot extract's potent antibacterial effect against Salmonella typhi, highlighting its therapeutic potential.
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2. Park SY, Kim HY. Effect of lyophilized chive (Allium wakegi Araki) supplementation to the frying batter mixture on quality attributes of fried chicken breast and tenderloin. Food Chem X 2022; 13: 100216.
3. Teshika JD, Zakariyyah AM, Zaynab T, Zengin G, Rengasamy KR, Pandian SK, et al. Traditional and modern uses of onion bulb (Allium cepa L.): a systematic review. Crit Rev Food Sci Nutr 2019; 59(sup1): S39-S70.
4. Zhao X-X, Lin F-J, Li H, Li H-B, Wu D-T, Geng F, et al. Recent advances in bioactive compounds, health functions, and safety concerns of onion (Allium cepa L.). Front Nutr 2021; 8: 669805.
5. Nassarawa SS, Nayik GA, Gupta SD, Areche FO, Jagdale YD, Ansari MJ, et al. Chemical aspects of polyphenol-protein interactions and their antibacterial activity. Crit Rev Food Sci Nutr 2023; 63: 9482-9505.
6. Asmilia N, Abrar M, Fahrimal Y, Sutriana A, Husna Y. Potential of malacca leaf (Phyllanthus emblica) against Salmonella sp. E3S Web Confer 2020; 151: 1-5.
7. Price LB, Hungate BA, Koch BJ, Davis GS, Liu CM. Colonizing opportunistic pathogens (COPs): The beasts in all of us. PLoS Pathog 2017; 13(8): e1006369.
8. Husain DR, Wardhani R. Antibacterial activity of endosymbiotic bacterial compound from Pheretima sp. Earthworms inhibit the growth of Salmonella Typhi and Staphylococcus aureus: in vitro and in silico approach. Iran J Microbiol 2021; 13: 537-543.
9. Breijyeh Z, Karaman R. Design and synthesis of novel antimicrobial agents. Antibiotics (Basel) 2023; 12: 628.
10. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health 2012; 2: 010401.
11. Sae-Yun A, Ovatlarnporn C, Itharat A, Wiwattanapatapee R. Extraction of rotenone from Derris elliptica and Derris malaccensis by pressurized liquid extraction compared with maceration. J Chromatogr A 2006; 1125: 172-176.
12. Mohammad A, Bhawani SA. Silica thin-layer chromatographic studies of surfactants with mixed aqueous-organic eluents containing thiourea: simultaneous separation of co-existing cetyltrimethylammonium bromide, dodecyltrimethylammonium bromide, and polyoxyethylene (20) sorbitan monolaurate. J Chromatogr Sci 2008; 46: 298-303.
13. Harlita TD, Oedjijono, Asnani A. The antibacterial activity of dayak onion (Eleutherine palmifolia (L.) merr) towards pathogenic bacteria. Trop Life Sci Res 2018; 29: 39-52.
14. Kumar D, Kumar V, Jangra P, Singh S. Leucas cephalotes (Spreng): photochemical investigation and antimicrobial activity via cylinder-plate method or cup-plate method. Int J Pharm Sci Res 2016; 1: 28-32.
15. Insrasari SD, Arofah D, Kristamtini, Sudarmaji, Handoko DD. Volatile compounds profile of some Indonesian shallot varieties. Earth Environ Sci 2021; 746: 012009.
16. Husain DR, Wardhani R, Erviani AE. Antibacterial activity of bacteria isolated from earthworm (Pheretima sp.) gut against Salmonella Typhi and Staphylococcus aureus: in vitro experiments supported by computational docking. Biodiversitas 2022; 23: 1125-1131.
17. Azwanida N. A review on the extraction methods use in medicinal plants, principle, strength and limitation. Med Aromat Plants 2015; 4: 1000196.
18. Fattorusso E, Iorizzi M, Lanzotti V, Taglialatela-Scafati O. Chemical composition of shallot (Allium ascalonicum hort.). J Agric Food Chem 2002; 50: 5686-5690.
19. Ruksiriwanich W, Khantham C, Muangsanguan A, Chittasupho C, Rachtanapun P, Jantanasakulwong K, et al. Phytochemical constitution, anti-inflammation, anti-androgen, and hair growth-promoting potential of shallot (Allium ascalonicum L.) extract. Plants (Basel) 2022; 11: 1499.
20. Omoba OS, Olagunju AI, Akinrinlola FO, Oluwajuyitan TD. Shallot‐enriched amaranth‐based extruded snack influences blood glucose levels, hematological parameters, and carbohydrate degrading enzymes in streptozotocin‐induced diabetic rats. J Food Biochem 2022; 46(11): e14098.
21. Jalal R, Bagheri SM, Moghimi A, Rasuli MB. Hypoglycemic effect of aqueous shallot and garlic extracts in rats with fructose-induced insulin resistance. J Clin Biochem Nutr 2007; 41: 218-223.
22. Hosseini FS, Falahati-Pour SK, Hajizadeh MR, Khoshdel A, Mirzaei MR, Ahmadirad H, et al. Persian shallot, Allium hirtifolium boiss, induced apoptosis in human hepatocellular carcinoma cells. Cytotechnology 2017; 69: 551-563.
23. Yang J, Meyers KJ, van der Heide J, Liu RH. Varietal differences in phenolic content and antioxidant and antiproliferative activities of onions. J Agric Food Chem 2004; 52: 6787-6793.
24. Ekowati J, Febriani K, Yaqin IN, Wulandari AA, Mulya IH, Nofianti KA, et al. Shallot skin rofiling, computational evaluation of physicochemical properties, ADMET, and molecular docking of its components against P2Y12 receptor. J Basic Clin Physiol Pharmacol 2021; 32: 429-437.
25. Bakht J, Khan S, Shafi M. Antimicrobial potentials of fresh Allium cepa against gram positive and gram negative bacteria and fungi. Pak J Bot 2013; 45: 1-6.
26. Hamza HJ. Antimicrobial activity of some plant extracts on microbial pathogens isolated from Hilla city hospitals, Iraq. Med J Babylon 2015; 12: 398-407.
27. Teshika JD, Zakariyyah AM, Zaynab T, Zengin G, Rengasamy KR, Pandian SK, et al. Traditional and modern uses of onion bulb (Allium cepa L.): a systematic review. Crit Rev Food Sci Nutr 2019; 59(sup1): S39-S70.
28. Matsuse K, Abdelrahman M, Ariyanti NA, Tsuji F, Hirata S, Nakajima, et al. Targeted metabolome profiling of Indonesian Shallots and Japanese long-day/short-day bulb onions. Metabolites 2022; 12: 1260.
29. Kyung KH. Antimicrobial properties of allium species. Curr Opin Biotechnol 2012; 23: 142-147.
30. Yan Y, Li X, Zhang C, Lv L, Gao B, Li M. Research progress on antibacterial activities and mechanisms of natural alkaloids: A review. Antibiotics (Basel) 2021; 10: 318.
31. Vollaro A, Esposito A, Antonaki E, Iula VD, D’Alonzo D, Guaragna A, et al. Steroid derivatives as potential antimicrobial agents against Staphylococcus aureus planktonic cells. Microorganisms 2020; 8: 468.
32. Bassolé IH, Juliani HR. Essential oils in combination and their antimicrobial properties. Molecules 2012; 17: 3989-4006.
33. Chandrasekaran M, Kannathasan K, Venkatesalu V. Antimicrobial activity of fatty acid methyl esters of some members of chenopodiaceae. Z Naturforsch C J Biosci 2008; 63: 331-336.
34. Starkenmann C, Niclass Y, Troccaz M. Nonvolatile S-Alk(en) ylthio-L-cysteine derivatives in fresh Onion (Allium cepa L. Cultivar). J Agric Food Chem 2011; 59: 9457-9465.
35. Breu W. Allium cepa L. (Onion) Part 1: Chemistry and analysis. Phytomedicine 1996; 3: 293-306.
36. Desbois AP. Potential applications of antimicrobial fatty acids in medicine, agriculture and other industries. Recent Pat Antiinfect Drug Discov 2012; 7: 111-122.
37. Bag A, Chattopadhyay RR. Evaluation of synergistic antibacterial and antioxidant efficacy of essential oils of spices and herbs in combination. PloS One 2015; 10(7): e0131321.
38. Ye CL, Dai DH, Hu WL. Antimicrobial and antioxidant activities of the essential oil from onion (Allium cepa L.). Food Control 2013; 30: 4853.
39. Abdel-Salam AF, Shahenda ME, Jehan BA. Antimicrobial and antioxidant activities of red onion, garlic and leek in sausage. Afr J Microbiol Res 2014; 8: 2574-2582.
40. Guedes IA, de Magalhães CS, Dardenne LE. Receptor–ligand molecular docking. Biophys Rev 2014; 6: 75-87.
41. Agarwal S, Chadha D, Mehrotra R. Molecular modeling and spectroscopic studies of semustine binding with DNA and its comparison with lomustine–DNA adduct formation. J Biomol Struct Dyn 2015; 33: 1653-1668.
42. Morgan RE, Batot GO, Dement JM, Rao VA, Eadsforth TC, Hunter WN. Crystal structures of Burkholderia cenocepacia dihydropteroate synthase in the apo-form and complexed with the product 7, 8-dihydropteroate. BMC Struct Biol 2011; 11: 21.
43. Hevener KE, Yun M-K, Qi J, Kerr ID, Babaoglu K, Hurdle JG, et al. Structural studies of pterin-based inhibitors of dihydropteroate synthase. J Med Chem 2010; 53: 166-177.
44. Yogavel M, Nettleship JE, Sharma A, Harlos K, Jamwal A, Chaturvedi R, et al. Structure of 6-hydroxymethyl-7, 8-dihydropterin pyrophosphokinase–dihydropteroate synthase from Plasmodium vivax sheds light on drug resistance. J Biol Chem 2018; 293: 14962-14972.
45. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. The penicillin-binding proteins: Structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 2008; 32: 234-258.
46. Azam MA, Thathan J, Jubie S. Dual targeting DNA gyrase B (GyrB) and topoisomerse IV (ParE) inhibitors: a review. Bioorg Chem 2015; 62: 41-63.
47. Rajendram M, Hurley KA, Foss MH, Thornton KM, Moore JT, Shaw JT, et al. Gyramides prevent bacterial growth by inhibiting DNA gyrase and altering chromosome topology. ACS Chem Biol 2014; 9: 1312-1319.
48. Karunanidhi A, Ghaznavi-Rad E, Hamat RA, Pichika MR, Lung LTT, Mohd Fauzi F, et al. Antibacterial and antibiofilm activities of nonpolar extracts of Allium stipitatum Regel. against multidrug resistant bacteria. Biomed Res Int 2018; 2018: 9845075.
49. Aghdam SZ, Minaeian S, Karimi MS, Bafroee AST. The antibacterial effects of the mixture of silver nanoparticles with the shallot and nettle alcoholic extracts. J Appl Biotechnol Rep 2019; 6: 158-164.
2. Park SY, Kim HY. Effect of lyophilized chive (Allium wakegi Araki) supplementation to the frying batter mixture on quality attributes of fried chicken breast and tenderloin. Food Chem X 2022; 13: 100216.
3. Teshika JD, Zakariyyah AM, Zaynab T, Zengin G, Rengasamy KR, Pandian SK, et al. Traditional and modern uses of onion bulb (Allium cepa L.): a systematic review. Crit Rev Food Sci Nutr 2019; 59(sup1): S39-S70.
4. Zhao X-X, Lin F-J, Li H, Li H-B, Wu D-T, Geng F, et al. Recent advances in bioactive compounds, health functions, and safety concerns of onion (Allium cepa L.). Front Nutr 2021; 8: 669805.
5. Nassarawa SS, Nayik GA, Gupta SD, Areche FO, Jagdale YD, Ansari MJ, et al. Chemical aspects of polyphenol-protein interactions and their antibacterial activity. Crit Rev Food Sci Nutr 2023; 63: 9482-9505.
6. Asmilia N, Abrar M, Fahrimal Y, Sutriana A, Husna Y. Potential of malacca leaf (Phyllanthus emblica) against Salmonella sp. E3S Web Confer 2020; 151: 1-5.
7. Price LB, Hungate BA, Koch BJ, Davis GS, Liu CM. Colonizing opportunistic pathogens (COPs): The beasts in all of us. PLoS Pathog 2017; 13(8): e1006369.
8. Husain DR, Wardhani R. Antibacterial activity of endosymbiotic bacterial compound from Pheretima sp. Earthworms inhibit the growth of Salmonella Typhi and Staphylococcus aureus: in vitro and in silico approach. Iran J Microbiol 2021; 13: 537-543.
9. Breijyeh Z, Karaman R. Design and synthesis of novel antimicrobial agents. Antibiotics (Basel) 2023; 12: 628.
10. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health 2012; 2: 010401.
11. Sae-Yun A, Ovatlarnporn C, Itharat A, Wiwattanapatapee R. Extraction of rotenone from Derris elliptica and Derris malaccensis by pressurized liquid extraction compared with maceration. J Chromatogr A 2006; 1125: 172-176.
12. Mohammad A, Bhawani SA. Silica thin-layer chromatographic studies of surfactants with mixed aqueous-organic eluents containing thiourea: simultaneous separation of co-existing cetyltrimethylammonium bromide, dodecyltrimethylammonium bromide, and polyoxyethylene (20) sorbitan monolaurate. J Chromatogr Sci 2008; 46: 298-303.
13. Harlita TD, Oedjijono, Asnani A. The antibacterial activity of dayak onion (Eleutherine palmifolia (L.) merr) towards pathogenic bacteria. Trop Life Sci Res 2018; 29: 39-52.
14. Kumar D, Kumar V, Jangra P, Singh S. Leucas cephalotes (Spreng): photochemical investigation and antimicrobial activity via cylinder-plate method or cup-plate method. Int J Pharm Sci Res 2016; 1: 28-32.
15. Insrasari SD, Arofah D, Kristamtini, Sudarmaji, Handoko DD. Volatile compounds profile of some Indonesian shallot varieties. Earth Environ Sci 2021; 746: 012009.
16. Husain DR, Wardhani R, Erviani AE. Antibacterial activity of bacteria isolated from earthworm (Pheretima sp.) gut against Salmonella Typhi and Staphylococcus aureus: in vitro experiments supported by computational docking. Biodiversitas 2022; 23: 1125-1131.
17. Azwanida N. A review on the extraction methods use in medicinal plants, principle, strength and limitation. Med Aromat Plants 2015; 4: 1000196.
18. Fattorusso E, Iorizzi M, Lanzotti V, Taglialatela-Scafati O. Chemical composition of shallot (Allium ascalonicum hort.). J Agric Food Chem 2002; 50: 5686-5690.
19. Ruksiriwanich W, Khantham C, Muangsanguan A, Chittasupho C, Rachtanapun P, Jantanasakulwong K, et al. Phytochemical constitution, anti-inflammation, anti-androgen, and hair growth-promoting potential of shallot (Allium ascalonicum L.) extract. Plants (Basel) 2022; 11: 1499.
20. Omoba OS, Olagunju AI, Akinrinlola FO, Oluwajuyitan TD. Shallot‐enriched amaranth‐based extruded snack influences blood glucose levels, hematological parameters, and carbohydrate degrading enzymes in streptozotocin‐induced diabetic rats. J Food Biochem 2022; 46(11): e14098.
21. Jalal R, Bagheri SM, Moghimi A, Rasuli MB. Hypoglycemic effect of aqueous shallot and garlic extracts in rats with fructose-induced insulin resistance. J Clin Biochem Nutr 2007; 41: 218-223.
22. Hosseini FS, Falahati-Pour SK, Hajizadeh MR, Khoshdel A, Mirzaei MR, Ahmadirad H, et al. Persian shallot, Allium hirtifolium boiss, induced apoptosis in human hepatocellular carcinoma cells. Cytotechnology 2017; 69: 551-563.
23. Yang J, Meyers KJ, van der Heide J, Liu RH. Varietal differences in phenolic content and antioxidant and antiproliferative activities of onions. J Agric Food Chem 2004; 52: 6787-6793.
24. Ekowati J, Febriani K, Yaqin IN, Wulandari AA, Mulya IH, Nofianti KA, et al. Shallot skin rofiling, computational evaluation of physicochemical properties, ADMET, and molecular docking of its components against P2Y12 receptor. J Basic Clin Physiol Pharmacol 2021; 32: 429-437.
25. Bakht J, Khan S, Shafi M. Antimicrobial potentials of fresh Allium cepa against gram positive and gram negative bacteria and fungi. Pak J Bot 2013; 45: 1-6.
26. Hamza HJ. Antimicrobial activity of some plant extracts on microbial pathogens isolated from Hilla city hospitals, Iraq. Med J Babylon 2015; 12: 398-407.
27. Teshika JD, Zakariyyah AM, Zaynab T, Zengin G, Rengasamy KR, Pandian SK, et al. Traditional and modern uses of onion bulb (Allium cepa L.): a systematic review. Crit Rev Food Sci Nutr 2019; 59(sup1): S39-S70.
28. Matsuse K, Abdelrahman M, Ariyanti NA, Tsuji F, Hirata S, Nakajima, et al. Targeted metabolome profiling of Indonesian Shallots and Japanese long-day/short-day bulb onions. Metabolites 2022; 12: 1260.
29. Kyung KH. Antimicrobial properties of allium species. Curr Opin Biotechnol 2012; 23: 142-147.
30. Yan Y, Li X, Zhang C, Lv L, Gao B, Li M. Research progress on antibacterial activities and mechanisms of natural alkaloids: A review. Antibiotics (Basel) 2021; 10: 318.
31. Vollaro A, Esposito A, Antonaki E, Iula VD, D’Alonzo D, Guaragna A, et al. Steroid derivatives as potential antimicrobial agents against Staphylococcus aureus planktonic cells. Microorganisms 2020; 8: 468.
32. Bassolé IH, Juliani HR. Essential oils in combination and their antimicrobial properties. Molecules 2012; 17: 3989-4006.
33. Chandrasekaran M, Kannathasan K, Venkatesalu V. Antimicrobial activity of fatty acid methyl esters of some members of chenopodiaceae. Z Naturforsch C J Biosci 2008; 63: 331-336.
34. Starkenmann C, Niclass Y, Troccaz M. Nonvolatile S-Alk(en) ylthio-L-cysteine derivatives in fresh Onion (Allium cepa L. Cultivar). J Agric Food Chem 2011; 59: 9457-9465.
35. Breu W. Allium cepa L. (Onion) Part 1: Chemistry and analysis. Phytomedicine 1996; 3: 293-306.
36. Desbois AP. Potential applications of antimicrobial fatty acids in medicine, agriculture and other industries. Recent Pat Antiinfect Drug Discov 2012; 7: 111-122.
37. Bag A, Chattopadhyay RR. Evaluation of synergistic antibacterial and antioxidant efficacy of essential oils of spices and herbs in combination. PloS One 2015; 10(7): e0131321.
38. Ye CL, Dai DH, Hu WL. Antimicrobial and antioxidant activities of the essential oil from onion (Allium cepa L.). Food Control 2013; 30: 4853.
39. Abdel-Salam AF, Shahenda ME, Jehan BA. Antimicrobial and antioxidant activities of red onion, garlic and leek in sausage. Afr J Microbiol Res 2014; 8: 2574-2582.
40. Guedes IA, de Magalhães CS, Dardenne LE. Receptor–ligand molecular docking. Biophys Rev 2014; 6: 75-87.
41. Agarwal S, Chadha D, Mehrotra R. Molecular modeling and spectroscopic studies of semustine binding with DNA and its comparison with lomustine–DNA adduct formation. J Biomol Struct Dyn 2015; 33: 1653-1668.
42. Morgan RE, Batot GO, Dement JM, Rao VA, Eadsforth TC, Hunter WN. Crystal structures of Burkholderia cenocepacia dihydropteroate synthase in the apo-form and complexed with the product 7, 8-dihydropteroate. BMC Struct Biol 2011; 11: 21.
43. Hevener KE, Yun M-K, Qi J, Kerr ID, Babaoglu K, Hurdle JG, et al. Structural studies of pterin-based inhibitors of dihydropteroate synthase. J Med Chem 2010; 53: 166-177.
44. Yogavel M, Nettleship JE, Sharma A, Harlos K, Jamwal A, Chaturvedi R, et al. Structure of 6-hydroxymethyl-7, 8-dihydropterin pyrophosphokinase–dihydropteroate synthase from Plasmodium vivax sheds light on drug resistance. J Biol Chem 2018; 293: 14962-14972.
45. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. The penicillin-binding proteins: Structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 2008; 32: 234-258.
46. Azam MA, Thathan J, Jubie S. Dual targeting DNA gyrase B (GyrB) and topoisomerse IV (ParE) inhibitors: a review. Bioorg Chem 2015; 62: 41-63.
47. Rajendram M, Hurley KA, Foss MH, Thornton KM, Moore JT, Shaw JT, et al. Gyramides prevent bacterial growth by inhibiting DNA gyrase and altering chromosome topology. ACS Chem Biol 2014; 9: 1312-1319.
48. Karunanidhi A, Ghaznavi-Rad E, Hamat RA, Pichika MR, Lung LTT, Mohd Fauzi F, et al. Antibacterial and antibiofilm activities of nonpolar extracts of Allium stipitatum Regel. against multidrug resistant bacteria. Biomed Res Int 2018; 2018: 9845075.
49. Aghdam SZ, Minaeian S, Karimi MS, Bafroee AST. The antibacterial effects of the mixture of silver nanoparticles with the shallot and nettle alcoholic extracts. J Appl Biotechnol Rep 2019; 6: 158-164.
| Files | ||
| Issue | Vol 16 No 2 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i2.15354 | |
| Keywords | ||
| Shallots; Antibacterial; Salmonella Typhi; Docking simulation | ||
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How to Cite
1.
Sari S, Wardhani R, Umar F, Husain D, Iwansyah A. Antibacterial activity of Shallots (Allium xwakegi Araki.) cultivars in Palu Valley against Salmonella Typhi ATCC 27870 through in vitro and in silico evaluation. Iran J Microbiol. 2024;16(2):208-218.
