Enhanced Bactericidal Effect of Enterocin A in Combination with Thyme Essential Oils Against L. Monocytogenes and E. Coli O157:H7

Overview

Journal J Food Sci Technol

Specialty Nutritional Sciences

Date 2015 Apr 2

PMID 25829595

Citations 8

Authors

Taoufik Ghrairi

Khaled Hani

Affiliations

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Abstract

The combined effects of enterocin A with Thymus vulgaris essential oils (EOs) against Listeria monocytogenes and Escherichia coli O157:H7 were investigated in vitro by enumeration of surviving populations of testing pathogens and minimal inhibitory concentration (MIC) determination. Enterocin A was purified to homogeneity by RP-HPLC from the culture fluid of Enterococcus strain and thyme EOs were extracted from local Thymus vulgaris plants. The major constituent of thyme EOs oils determined by GC-MS was thymol (78.4 %). Combination of enterocin A with thyme EOs showed an enhanced bactericidal effect against Listeria monocytogenes. Checkerboard assay and isobologram construction displayed a synergistic interaction between these compounds against Listeria (FIC index <0.5). Moreover, the MIC value of enterocin A has fallen fivefold (from 4.57 to 0.9 μg/ml), while the MIC of thyme EOs decreased threefold (from 3.6 to 1.2 μg/ml). Treatments with enterocin A alone did not affect the growth of the enteric pathogen E. coli O157:H7. However, the addition of thyme EOs and enterocin A yielded a synergistic antimicrobial effect against E. coli (MIC thyme EOs decrease from 2.2 to 0.71 μg/ml). This is the first report on the combined effect of enterocin A and thyme EOs against food pathogen bacteria. This combination could be useful in food bio-preservation.

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References

Friedly E, Crandall P, Ricke S, Roman M, OBryan C, Chalova V . In vitro antilisterial effects of citrus oil fractions in combination with organic acids. J Food Sci. 2009; 74(2):M67-72. DOI: 10.1111/j.1750-3841.2009.01056.x. View

Morisset D, Berjeaud J, Marion D, Lacombe C, Frere J . Mutational analysis of mesentericin y105, an anti-Listeria bacteriocin, for determination of impact on bactericidal activity, in vitro secondary structure, and membrane interaction. Appl Environ Microbiol. 2004; 70(8):4672-80. PMC: 492324. DOI: 10.1128/AEM.70.8.4672-4680.2004. View

Janes M, Nannapaneni R, Johnson M . Identification and characterization of two bacteriocin-producing bacteria isolated from garlic and ginger root. J Food Prot. 1999; 62(8):899-904. DOI: 10.4315/0362-028x-62.8.899. View

Thompson J, Chalchat J, Michet A, Linhart Y, Ehlers B . Qualitative and quantitative variation in monoterpene co-occurrence and composition in the essential oil of Thymus vulgaris chemotypes. J Chem Ecol. 2003; 29(4):859-80. DOI: 10.1023/a:1022927615442. View

Kim E, Choi N, Bajpai V, Kang S . Synergistic effect of nisin and garlic shoot juice against Listeria monocytogenes in milk. Food Chem. 2015; 110(2):375-82. DOI: 10.1016/j.foodchem.2008.02.013. View

Ghrairi T, Manai M, Berjeaud J, Frere J . Antilisterial activity of lactic acid bacteria isolated from rigouta, a traditional Tunisian cheese. J Appl Microbiol. 2004; 97(3):621-8. DOI: 10.1111/j.1365-2672.2004.02347.x. View

Borrero J, Kunze G, Jimenez J, Boer E, Gutiez L, Herranz C . Cloning, production, and functional expression of the bacteriocin enterocin A, produced by Enterococcus faecium T136, by the yeasts Pichia pastoris, Kluyveromyces lactis, Hansenula polymorpha, and Arxula adeninivorans. Appl Environ Microbiol. 2012; 78(16):5956-61. PMC: 3406115. DOI: 10.1128/AEM.00530-12. View

Solomakos N, Govaris A, Koidis P, Botsoglou N . The antimicrobial effect of thyme essential oil, nisin, and their combination against Listeria monocytogenes in minced beef during refrigerated storage. Food Microbiol. 2007; 25(1):120-7. DOI: 10.1016/j.fm.2007.07.002. View

Aymerich T, Holo H, Havarstein L, Hugas M, Garriga M, Nes I . Biochemical and genetic characterization of enterocin A from Enterococcus faecium, a new antilisterial bacteriocin in the pediocin family of bacteriocins. Appl Environ Microbiol. 1996; 62(5):1676-82. PMC: 167941. DOI: 10.1128/aem.62.5.1676-1682.1996. View

10.

VANDENDOOL H, KRATZ P . A GENERALIZATION OF THE RETENTION INDEX SYSTEM INCLUDING LINEAR TEMPERATURE PROGRAMMED GAS-LIQUID PARTITION CHROMATOGRAPHY. J Chromatogr. 1963; 11:463-71. DOI: 10.1016/s0021-9673(01)80947-x. View

11.

Church D . Major factors affecting the emergence and re-emergence of infectious diseases. Clin Lab Med. 2004; 24(3):559-86, v. PMC: 7119055. DOI: 10.1016/j.cll.2004.05.008. View

12.

Burt S . Essential oils: their antibacterial properties and potential applications in foods--a review. Int J Food Microbiol. 2004; 94(3):223-53. DOI: 10.1016/j.ijfoodmicro.2004.03.022. View

13.

Martin M, Gutierrez J, Criado R, Herranz C, Cintas L, Hernandez P . Cloning, production and expression of the bacteriocin enterocin A produced by Enterococcus faecium PLBC21 in Lactococcus lactis. Appl Microbiol Biotechnol. 2007; 76(3):667-75. DOI: 10.1007/s00253-007-1044-3. View

14.

Johnson M, MacDougall C, Ostrosky-Zeichner L, Perfect J, Rex J . Combination antifungal therapy. Antimicrob Agents Chemother. 2004; 48(3):693-715. PMC: 353116. DOI: 10.1128/AAC.48.3.693-715.2004. View

15.

Antonio C, Abriouel H, Lopez R, Ben Omar N, Valdivia E, Galvez A . Enhanced bactericidal activity of enterocin AS-48 in combination with essential oils, natural bioactive compounds and chemical preservatives against Listeria monocytogenes in ready-to-eat salad. Food Chem Toxicol. 2009; 47(9):2216-23. DOI: 10.1016/j.fct.2009.06.012. View

16.

Orhan G, Bayram A, Zer Y, Balci I . Synergy tests by E test and checkerboard methods of antimicrobial combinations against Brucella melitensis. J Clin Microbiol. 2005; 43(1):140-3. PMC: 540140. DOI: 10.1128/JCM.43.1.140-143.2005. View

17.

Boziaris I, Adams M . Effect of chelators and nisin produced in situ on inhibition and inactivation of gram negatives. Int J Food Microbiol. 2000; 53(2-3):105-13. DOI: 10.1016/s0168-1605(99)00139-7. View

18.

Eloff J . A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med. 1999; 64(8):711-3. DOI: 10.1055/s-2006-957563. View

19.

Moore J, Corcoran D, Dooley J, Fanning S, Lucey B, Matsuda M . Campylobacter. Vet Res. 2005; 36(3):351-82. DOI: 10.1051/vetres:2005012. View

20.

Hernandez T, Canales M, Avila J, Garcia A, Martinez A, Caballero J . Composition and antibacterial activity of essential oil of Lantana achyranthifolia Desf. (Verbenaceae). J Ethnopharmacol. 2004; 96(3):551-4. DOI: 10.1016/j.jep.2004.09.044. View