Antimicrobial Activity of Chemical Substances Derived from S-Alk(en)yl-L-Cysteine Sulfoxide (Alliin) in Garlic, Allium sativum L.

  • Published : 2007.02.28

Abstract

Garlic (Allium sativum L.) contains a specific sulfur compound, the S-allyl derivative of L-cysteine sulfoxide, and has long been known for its antimicrobial activity against various microorganisms, including bacteria, fungi, and protozoa. The principal antimicrobial compound of garlic is S-allyl-L-propenethiosulfinate (allicin) which is generated by an enzyme, alliinase (L-cysteine sulfoxide lyase), from S-allyl-L-cysteine sulfoxide (alliin). This compound exists exclusively in Allium as a major non-protein sulfur-containing amino acid. S-Allyl-L-propenethiosulfinate belongs to the chemical group of thiosulfinates and is a highly potent antimicrobial. The potency of garlic extract is reduced during storage since thiosulfinates are unstable and are degraded to other compounds some of which do not have antimicrobial activity. Diallyl polysulfides and ajoene are sulfur compounds derived from allicin that do possess antimicrobial activity. It was recently found that garlic becomes antimicrobial on heating at cooking temperatures, and that the compound responsible for this is allyl alcohol, which is generated from alliin by thermal degradation.

Keywords

References

  1. Walton L, Herbold M, Lindegren CC. Bactericidal effects of vapors from crushed garlic. Food Res. 1: 163-169 (1936) https://doi.org/10.1111/j.1365-2621.1936.tb17778.x
  2. Sherman JM, Hodge HM. The bactericidal properties of certain plant juices. J. Bacteriol. 31: 96 (1936)
  3. Cavallito CJ, Bailey JH. Allicin, the antibacterial principle of Allium sativum. I: Isolation, physical properties and antimicrobial action. J. Am. Chem. Soc. 66: 1950-1951 (1944) https://doi.org/10.1021/ja01239a048
  4. Stoll A, Seebeck E. Chemical investigation of alliin, the specific principle of garlic. Adv. Enzymol. 11: 377-400 (1951)
  5. Kyung KH, Fleming HP. S-Methyl-L-cysteine sulfoxide as the precursor of methyl methanethiosulfinate, the principal antibacterial compound in cabbage. J. Food Sci. 59: 350-355. (1994) https://doi.org/10.1111/j.1365-2621.1994.tb06964.x
  6. Virtanen AI. Some organic sulfur compounds in vegetables and fodder plants and their significance in human nutrition. Angew. Chem. Int. Edit. 6: 299-306 (1962)
  7. Zsolnai VT. The antimicrobial action of thiocyanates and isothiocyanates. Int. Mitteilung, Arzneim. Forsch., 16: 870-876 (1966)
  8. Delaquis PJ, Mazza G. Antimicrobial properties of isothiocyanates in food preservation. Food Technol.-Chicago 49: 73-84 (1995)
  9. Virtanen AI. Studies on organosulfur compounds and other labile substances in plants. Phytochemistry 4: 207-228 (1965) https://doi.org/10.1016/S0031-9422(00)86168-3
  10. Synge RLM, Wood JC. (+)-S-Methyl-L-cysteine s-oxide in cabbage. Biochem. J. 64: 252-259 (1956) https://doi.org/10.1042/bj0640252
  11. Morris CJ, Thompson JF. The identification of (+)S-methyl-L-cysteine sulfoxide in plants. J. Am. Chem. Soc. 78: 1605-1608 (1956) https://doi.org/10.1021/ja01589a028
  12. Marks HS, Hilson JA, Leichtweis HC, Stoewsand GS. S-Methylcysteine sulfoxide in Brassica vegetables and formation of methyl methanethiosulfinate from Brussels sprout. J. Agr. Food Chem. 40: 2098-2101 (1992) https://doi.org/10.1021/jf00023a012
  13. Block E, Naganathan S, Putman D, Zhao S-H. Allium chemistry: HPLC analysis of thiosulfinates from onion, garlic, wild garlic (Ram sons), leek, scallion, shallot, elephant (great-headed) garlic chive, and Chinese chive. J. Agr. Food Chem. 40: 2418-2430 (1992) https://doi.org/10.1021/jf00024a017
  14. Stoll A, Seebeck E. About alliin, the genuine mother substance of garlic. 1. Communication about Alliium sunstance. Helv. Chim. Acta 31: 189-210 (1948) https://doi.org/10.1002/hlca.19480310140
  15. Rundqvist C. Pharmacological investigation of Allium bulbs. Pharmaceutiskt Notisblad. 18: 323-333 (1909)
  16. Stoll A, Seebeck E. Synthesis of natural alliin and its three optically active isomers. 5. Communication about Allium-substance. Helv. Chim. Acta 34: 481-487 (1951) https://doi.org/10.1002/hlca.19510340212
  17. Marks HS. Isolation, identification, and genotoxic inhibitory efficacy of naturally occurring organosulfur compounds present in Brassica vegetables. PhD thesis, Cornell University Ithaca NY USA (1992)
  18. Caragay AB. Cancer-preventive foods and ingredients. Food Technol.-Chicago 46: 65-68 (1992)
  19. Alberto-Puleo M. Physiological effects of cabbage with reference to its potential as a dietary cancer-inhibitor and its use in ancient medicine. J. Ethnopharmacol. 9: 261-272 (1983) https://doi.org/10.1016/0378-8741(83)90035-1
  20. Augusti KT, Mathew PT. Lipid lowering effect of allicin (diallyl disulphide-oxide) on long term feeding to normal rats. Experientia 30: 468-470 (1974) https://doi.org/10.1007/BF01926297
  21. Rees LP, Minney SF, Plummer NT, Slator JH, Skyrme DA. A quantitative assessment of the antimicrobial activity of garlic (Allium sativum). World J. Microb. Biot. 9: 303-307 (1993) https://doi.org/10.1007/BF00383068
  22. Block E, Ahmed S, Jain MK, Creely RW, Apitz-Castro R, Cruz MR. (E,Z)-Ajoene: A potent antithrombotic agent from garlic. J. Am. Chem. Soc. 106: 8295-8296 (1984) https://doi.org/10.1021/ja00338a049
  23. Wills ED. Enzyme inhibition by allicin, the active principle of garlic. Biochem. J. 63: 514-520 (1956) https://doi.org/10.1042/bj0630514
  24. Adetumbi M, Javor GT, Lau BHS. Allium sativum (garlic) inhibits lipid synthesis in Candida albicans. Antimicrob. Agents Ch. 30: 499-501 (1986) https://doi.org/10.1128/AAC.30.3.499
  25. Ghannoum MA. Studies of the antimicrobial mode of action of Allium sativum (garlic). J. Gen. Microbiol. 134: 2917-2924 (1988)
  26. Feldberg RS, Chang SC, Kotik AN, Nadler M, Neuwirth Z, Sundstrom DC, Thompson NH. In vitro mechanism of inhibition of bacterial cell growth by allicin. Antimicrob. Agents Ch. 32: 1763-1768 (1988) https://doi.org/10.1128/AAC.32.12.1763
  27. Focke M, Feld A, Lichtenthaler HK. Allicin, a naturally occurring antibiotic from garlic, specifically inhibits acetyl-CoA synthetase. FEBS 261: 106-108 (1990) https://doi.org/10.1016/0014-5793(90)80647-2
  28. Dababneh FA, Al-Delaimy KS. Inhibition of Staphylococcus aureus by garlic extract. Lebensm. -Wiss. Technol. 17: 29-31 (1984)
  29. Karaioannoglou PG, Mantis AJ, Panetos AG The effects of garlic extract on lactic acid bacteria (Lactobacillus plantarum) in culture media. Lebensm. - Wiss. Technol. 10: 148-150 (1977)
  30. Mantis AJ, Karaioannoglou PG, Spanos GP, Panetos AG The effect of garlic extract on food poisoning bacteria in culture media. I. Staphylococcus aureus. Lebensm. - Wiss. Technol. 11: 26-28 (1978)
  31. Conner DE, Beuchat LR. Effects of essential oils from plants on growth of food spoilage yeasts J. Food Sci. 49: 429-434 (1984) https://doi.org/10.1111/j.1365-2621.1984.tb12437.x
  32. Johnson MG, Vaughn RH. Death of Salmonella typhimurium and Escherichia coli in the presence of freshly reconstituted dehydrated garlic and onion. Appl. Microbiol. 17: 903-905 (1969)
  33. Saleem ZM, Al-Delaimy KS. Inhibition of Bacillus cereus by garlic extracts. J. Food Protect. 45: 1007-1009 (1982) https://doi.org/10.4315/0362-028X-45.11.1007
  34. DeWit JC, Notermans S, Gorin N, Kampelmacher EH. Effects of garlic oil or onion oil on toxin production by Clostridium botulinum in meat slurry. J. Food Protect. 42: 222-224 (1979) https://doi.org/10.4315/0362-028X-42.3.222
  35. Mantis AJ, Koidis PA, Karaioannoglou PG, Panetos AG. Effect of garlic extract on food poisoning bacteria. Lebensm. - Wiss. Technol. 12: 230-232 (1979)
  36. Barone FE, Tansey MR. Isolation, purification, identification, synthesis, and kinetics of activity of the anticandidal component of Allium sativum, and a hypothesis for its mode of action. Mycologia 69: 793-825 (1977) https://doi.org/10.2307/3758870
  37. Al-Delaimy KS, Ali SH. Antibacterial action of vegetable extracts on the growth of pathogenic bacteria. J. Sci. Food Agr. 21: 110-112 (1970) https://doi.org/10.1002/jsfa.2740210214
  38. Srivastava KC, Perera AD, Saridakis HO. Bacteriostatic effects of garlic sap on Gram negative pathogenic bacteria: An in vitro study. Lebensm. -Wiss. Technol. 15: 74-76 (1982)
  39. Moore GS, Atkins RD. The fungicidal and fungistatic effects of aqueous garlic extract on medically important yeast-like fungi. Mycologia 69: 341-348 (1977) https://doi.org/10.2307/3758659
  40. Tansey MR. Appleton JA. Inhibition of fungal growth by garlic extract. Mycologia 67: 409-413 (1975) https://doi.org/10.2307/3758431
  41. Kyung KH, Kim MH, Park MS, Kim YS. Alliinase-independent inhibition of Staphylococus aureus B33 by heated garlic. J. Food Sci. 67: 780-785 (2002) https://doi.org/10.1111/j.1365-2621.2002.tb10676.x
  42. Singh KV, Shukula NP. Activity of multiple resistant bacteria of garlic (Allium sativum) extract. Fitoterapia 15: 313-315 (1984)
  43. Hamamoto A, Mazelis M. The C-S lyases of higher plants; Isolation and properties of homogeneous cystine lyase from broccoli. Plant Physiol. 80: 702-706 (1986) https://doi.org/10.1104/pp.80.3.702
  44. Mae T, Ohira K, Fujiwara A. Fate of (+)S-methyl-L-cysteine sulfoxide in Chinese cabbage, Brassica pekinesis RUPR. Plant Cell Physiol. 12: 1-11 (1971) https://doi.org/10.1093/oxfordjournals.pcp.a074591
  45. Kyung KH, Fleming HP. Antibacterial activity of cabbage juice against lactic acid bacteria. J. Food Sci. 59: 125-129 (1994) https://doi.org/10.1111/j.1365-2621.1994.tb06915.x
  46. Ziegler SJ, Stitcher O. HPLC of S-alk(en)yl-L-cysteine derivatives in garlic including quantitative determination of (+)S-allyl-L-cysteine sulfoxide (alliin). Planta Med. 55: 372-377 (1989) https://doi.org/10.1055/s-2006-962031
  47. Freeman GG, Whenham RJ. The use of synthetic (+/-)-S-I-propyl-Lcysteine sulphoxide and of alliinase preparations in studies of flavour changes resulting from processing of onion (Allium cepa L.). J. Sci. Food Agr. 26: 1333-1346 (1975) https://doi.org/10.1002/jsfa.2740260912
  48. Kunelius HT, Sanderson JB, Narashimhalu PR. Effect of seeding date on yields and quality of green forage crops. Can. J. Plant Sci. 67: 1045-1050 (1987) https://doi.org/10.4141/cjps87-140
  49. Bradshaw JE, Borzucki R. Digestability, S-methyl-L-cysteine sulfoxide content and thiocyante ion content of cabbage of stockfeeding. J. Sci. Food Agr. 33: 1-5 (1982) https://doi.org/10.1002/jsfa.2740330102
  50. Fujiwara M, Yoshimura M, Tsuno S, Murakami F. 'Allithiamine,' a newly found derivative of vitamin BI. IV. On the allicin homologues in the vegetables. J. Biochem. -Tokyo 45: 141-149 (1958) https://doi.org/10.1093/oxfordjournals.jbchem.a126850
  51. Horhammer L, Wagner H, Seitz M, Vejdelek ZJ. Onion flavors and their analysis by gas chromatography-mass spectrometry. Pharmazie 23: 462-466 (1968)
  52. Lawson LD. Garlic: A review of its medicinal effects and indicated active compounds. pp. 176-209. In: Phytomedicines of Europe: Their Chemistry & Biological Activity. Lawson LD, Bauer R (eds). ACS Symposium Series 691, American Chemical Society, Washington, DC, USA (1998)
  53. Nomura J, Nishizuka Y, Hayaishi O. S-Alkylcysteinase: Enzymatic cleavage of s-methyl-L-cysteine and its sulfoxide. J. Biol. Chem. 238: 1441-1446 (1963)
  54. Murakami F. Studies on the nutritional value of Allium Plants (XXXVI) Decomposition of alliin homologues by microorganism and formation of substance with thiamine masking activity. Vitamins (Tokyo) 20: 126 (1960)
  55. Smith RH. Kale Poisoning: The Brassica anaemia factor. Vet. Rec. 107: 12-15 (1980) https://doi.org/10.1136/vr.107.1.12
  56. Cavallito CJ, Buck JS, Suter CM. Allicin, the antibacterial principles of Allium sativim. II. Determination of the chemical structure. J. Am. Chem. Soc. 66: 1952-1954 (1944) https://doi.org/10.1021/ja01239a049
  57. Block E. Flavor artifacts. J. Agr. Food Chem. 41: 692 (1993)
  58. Brodnitz MH, Pascale JV, von Derslice L. Flavor components of garlic extract. J. Agr. Food Chem. 19: 273-275 (1971) https://doi.org/10.1021/jf60174a007
  59. Yu T-H, Wu C-M. Stability of allicin in garlic juice. J. Food Sci. 54: 977-981 (1989) https://doi.org/10.1111/j.1365-2621.1989.tb07926.x
  60. Small LD, Bailey JH, Cavallito CJ. Alkyl thiosulfinates. J. Am. Chem. Soc. 69: 1710-1713 (1947) https://doi.org/10.1021/ja01199a040
  61. Kim JW, Kyung KH. Antiyeast activity of heated garlic in the absence of alliinase enzyme action. J. Food Sci. 68: 1766-1770 (2003) https://doi.org/10.1111/j.1365-2621.2003.tb12326.x
  62. Ingersoll RL, Volirath RE, Scott B, Lindegren CC. Bactericidal activity of crotonaldehyde. Food Res. 3: 389-392 (1938) https://doi.org/10.1111/j.1365-2621.1938.tb17072.x
  63. Small LD, Bailey JH, Cavallito CJ. Comparison of some properties of thiosulfonates and thiosulfinates. J. Am. Chem. Soc. 71: 3565-3566 (1949) https://doi.org/10.1021/ja01178a531
  64. Yoshida S, Kasuga S, Hayashi N, Ushiroguchi T, Matsuura H, Nakagawa S. Antifungal activity of ajoene derived from garlic. Appl. Environ. Microbiol. 53: 615-617 (1987)
  65. Naganawa R, Iwata N, Ishikawa K, Fukyda H, Fujino T, Suzuki A. Inhibition of microbial growth by ajoene, a sulfur-containg compound derived from garlic. Appl. Environ. Microbiol. 62: 4238-4242 (1996)
  66. Brown HD, Matzuk AR, Becker HJ, Conbere JP, Constantin JM, Solotorovsky M, Winsten S, Ironson E, Quastel JH. The antituberculosis activity of some ethylmercapto compounds. J. Am. Chem. Soc. 76: 3860 (1954)
  67. Kubelik J. Antimicrobial properties of garlic. Pharmazie 25: 266-269 (1970)
  68. Lubeck VL. Method of stabilization of antibiotic effective ingredient of Allium sativum. Deutsch. Pat. 943250 (1956)
  69. Lawson LD. The composition and chemistry of garlic cloves and processed garlic. pp. 37-107. In: Garlic, The Science and Therapeutic Applications of Allium sativum L. and Related Species. 2nd ed. Koch HP, Lawson LD (eds). Williams & Wilkins, Baltimore, MD, USA (1996)
  70. Kim JW, Huh JE, Kyung SH, Kyung KH. Antimicrobial activity of alk(en)yl sulfides found in essential oils of garlic and onion. Food Sci. Biotechnol. 13: 235-239 (2004)
  71. Choi JH, Kyung KH. Allyl alcohol is the sole antiyeast compound in heated garlic extract. J. Food Sci. 70: M305-M309 (2005) https://doi.org/10.1111/j.1365-2621.2005.tb11452.x
  72. Pentz R, Siegers CP. Garlic preparations: Methods for quantitative and qualitative assessment of their ingredients. pp. 109-134. In: Garlic, The Science and Therapeutic Applicatiollof Allium sativum L. and Related Species. 2nd ed. Koch HP, Lawson LD (eds). Williams & Wilkins, Baltimore, MD, USA (1996)
  73. O'Gara EA, Hill DJ, Maslin DJ. Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Appl. Environ. Microbiol. 66: 2269-2273 (2000) https://doi.org/10.1128/AEM.66.5.2269-2273.2000
  74. Kim JW, Kim YS, Kyung KH. Inhibitory activity of essential oils of garlic and onion against bacteria and yeasts. J. Food Protect. 67: 499-504 (2004) https://doi.org/10.4315/0362-028X-67.3.499
  75. Lawson LD, Wang ZJ, Hughes BG. Identification and HPLC analysis of sulfides and dialk(en)yl thiosulfinates in commercial garlic products. Planta Med. 57: 363-370 (1991) https://doi.org/10.1055/s-2006-960119
  76. Ross ZM, O'Gara EA, Hill DJ, Sieighttholme HV, Maslin DJ. Antimicrobial properties of garlic oil against human enteric bacteria: Evaluation of methodologies and comparisons with garlic oil sulfides and garlic powder. Appl. Environ. Microbiol. 67: 475-480 (2001) https://doi.org/10.1128/AEM.67.1.475-480.2001
  77. Lee S, Woo YH, Kyung KH. Allyl alcohol found in heated garlic is a potent selective inhibitor for yeasts but not for bacteria. J. Microbiol. Biotechn. 16: 1236-1239 (2006)
  78. Youngleson JS, Santangelo JD, Jones DT, Woods DR. Cloning and expression of a Clostridium acetobutylicum alchohol dehyadrogease gene in Escherichia coli. Appl. Environ. Microbiol. 54: 676-682 (1988)
  79. Rando RR. Allyl alcohol-induced irreversible inhibition of yeast alcohol dehydrogenase. Biochem. Pharmacol. 23: 2328-2331 (1974) https://doi.org/10.1016/0006-2952(74)90563-2
  80. Dickinson F, Dalziel K. The specifications and configurations of ternary complexes of yeast and liver alcohol dehydrogenases. Biochem. J., 104: 165-172 (1967) https://doi.org/10.1042/bj1040165
  81. Lorowitz W, Clark D. Escherichia coli mutants with a temperaturesensitive alcohol dehydrogenase. J. Bacteriol. 152: 935-938 (1982)
  82. Al-Delaimy KS, Barakat MMF. Antimicrobial and preservative activity of garlic on fresh ground camel meat. 1. Effect of fresh ground garlic segments. J. Sci. Food Agr. 22: 96-98 (1971) https://doi.org/10.1002/jsfa.2740220214
  83. Le Dinh H, Kyung KH. Inhibition of yeast film formation in fermented vegetables by materials derived from garlic using cucumber pickle fermentation as model system. Food Sci. Biotechnol. 15: 469-473 (2006)
  84. Moon B-Y, Lee E-J, Park J-H. Characteristics of antibiotic resistance of foodborne pathogens adapted to garlic, Allium sativum L. Food Sci. Biotechnol. 15: 511-515 (2006)