Characterization of the action of selected essential oil components on Gram-negative bacteria
Open accessAbstract
Carvacrol, (+)-carvone, thymol, and trans -cinnamaldehyde were tested for their inhibitory activity against Escherichia coli O157:H7 and Salmonella typhimurium . In addition, their toxicity to Photobacterium leiognathi was determined, utilizing a bioluminescence assay. Their effects on the cell surface were investigated by measuring the uptake of 1- N -phenylnaphthylamine (NPN), by measuring their sensitization of bacterial suspensions toward detergents and lysozyme, and by analyzing material released from cells upon treatment by these agents. Carvacrol, thymol, and trans -cinnamaldehyde inhibited E. coli and S. typhimurium at 1−3 mM, whereas (+)-carvone was less inhibitory. trans -Cinnamaldehyde was the most inhibitory component toward P. leiognathi . Carvacrol and thymol disintegrated the outer membrane and released outer membrane-associated material from the cells to the external medium; such release by (+)-carvone or trans -cinnamaldehyde was negligible. Of the tested components, carvacrol and thymol decreased the intracellular ATP pool of E. coli and also inreased extracellular ATP, indicating disruptive action on the cytoplasmic membrane. Keywords: Essential oils; carvacrol; carvone; cinnamaldehyde; thymol; antimicrobial activity; outer membrane; lipopolysaccharide
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Carvacrol's effect on membrane permeability was confirmed by monitoring the efflux of H+, K+, carboxyfluorescein and ATP and the influx of nucleic acid stains.
“Carvacrol’s effect on membrane permeability was confirmed monitoring the efflux of H+, K+, carboxyfluorescein and ATP and the influx of nucleic acid stains [13,20,24,28,36].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [13]
Non-specific inhibition of membrane-bound or -embedded enzymes can be caused by small hydrophobic molecules as a result of changes in protein conformation.
“Non-specific inhibition of membrane-bound or -embedded enzymes can be caused by small hydrophobic molecules as a result of changes in the protein conformation.”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [13]
Cites
Escherichia coli and Salmonella :cellular and molecular biology
Neidhardt, F. C. (1996) · ASM Press eBooks · Cited by 8,230 · see citing works
Mechanisms of membrane toxicity of hydrocarbons
Sikkema, J., de Bont, J. A., & Poolman, B. (1995) · Microbiological Reviews · doi:10.1128/mr.59.2.201-222.1995 · Cited by 2,685 · see citing works
Agents that increase the permeability of the outer membrane
Vaara, M. (1992) · Microbiological Reviews · doi:10.1128/mr.56.3.395-411.1992 · Cited by 1,879 · see citing works
Prevention of Drug Access to Bacterial Targets: Permeability Barriers and Active Efflux
Nikaido, H. (1994) · Science · doi:10.1126/science.8153625 · Cited by 1,542 · see citing works
Antibacterial properties of plant essential oils
Deans, S. G., & Ritchie, G. Y. (1987) · International Journal of Food Microbiology · doi:10.1016/0168-1605(87)90034-1 · Cited by 875 · see citing works
Juven, B. J., Kanner, J., Schved, F., & Weisslowicz, H. (1994) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1994.tb01661.x · Cited by 833 · see citing works
Resistance to Antibiotics Mediated by Target Alterations
Spratt, B. G. (1994) · Science · doi:10.1126/science.8153626 · Cited by 673 · see citing works
Antimicrobial and Cytotoxic Activities of Origanum Essential Oils
Sivropoulou, A., Papanikolaou, E., Nikolaou, C., Kokkini, S., Λαναράς, Θ., & Arsenakis, M. (1996) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf950540t · Cited by 666 · see citing works
Molecular basis of bacterial outer membrane permeability
Nikaido, H., & Vaara, M. (1985) · Microbiological Reviews · doi:10.1128/mr.49.1.1-32.1985 · Cited by 553 · see citing works
Loh, B. A., Grant, C. W. M., & Hancock, R. E. W. (1984) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.26.4.546 · Cited by 494 · see citing works
Potential of lactic acid bacteria and novel antimicrobials against Gram-negative bacteria
Helander, I. M., von Wright, A., & Mattila-Sandholm, T. (1997) · Trends in Food Science & Technology · doi:10.1016/s0924-2244(97)01030-3 · Cited by 306 · see citing works
Self-citationPolyethyleneimine is an effective permeabilizer of Gram negative bacteria
Helander, I. M., Alakomi, H.-L., Latva-Kala, K., & Koski, P. (1997) · Microbiology · doi:10.1099/00221287-143-10-3193 · Cited by 237 · see citing works
Self-citationInhibition of foodborne pathogens by thymol, eugenol, menthol and anethole
Karapınar, M., & Aktuğ, Ş. E. (1987) · International Journal of Food Microbiology · doi:10.1016/0168-1605(87)90023-7 · Cited by 227 · see citing works
Lundin, A., & Thore, A. (1975) · Analytical Biochemistry · doi:10.1016/0003-2697(75)90723-x · Cited by 225 · see citing works
Zähringer, U., Lindner, B., & Rietschel, E. (1994) · Advances in carbohydrate chemistry and biochemistry · doi:10.1016/s0065-2318(08)60152-3 · Cited by 216 · see citing works
Outer membranes of Gram‐negative bacteria are permeable to steroid probes
Plésiat, P., & Nikaido, H. (1992) · Molecular Microbiology · doi:10.1111/j.1365-2958.1992.tb00853.x · Cited by 191 · see citing works
Moore, L. V. H., BOURNE, D. M., & Moore, W. E. (1994) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-44-2-338 · Cited by 153 · see citing works
Phenol-induced membrane changes in free and immobilized Escherichia coli
Keweloh, H., Weyrauch, G., & Rehm, H. J. (1990) · Applied Microbiology and Biotechnology · doi:10.1007/bf00170572 · Cited by 147 · see citing works
Energy recycling by lactate efflux in growing and nongrowing cells of Streptococcus cremoris
ten Brink, B., Otto, R., Hansen, U., & Konings, W. N. (1985) · Journal of Bacteriology · doi:10.1128/jb.162.1.383-390.1985 · Cited by 102 · see citing works
Helander, I. M., & Haikara, A. (1995) · Microbiology · doi:10.1099/13500872-141-5-1131 · Cited by 31 · see citing works
Self-citationOosterhaven, K., Leitao, A. C., Gorris, L. G. M., et al. (1996) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1996.tb03253.x · Cited by 29 · see citing works
Self-citationFungicidal and fungistatic action of the secondary plant metabolites cinnarnaldehyde and carvone
Smid, E. J., Koeken, J. G. P., & Gorris, L. G. M. (1996) · Socio-Environmental Systems Modeling · Cited by 14 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Essential oils: Their antibacterial properties and potential applications in foods—A review
Burt, S. (2004) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.03.022 · Cited by 10,488 · see citing works
Biological effects of essential oils—A review
Bakkali, F., Averbeck, S., Averbeck, D., & Idaomar, M. (2008) · Food and Chemical Toxicology · doi:10.1016/j.fct.2007.09.106 · Cited by 7,929 · see citing works
Lambert, R. J. W., Skandamis, P. N., Coote, P. J., & Nychas, G.-J. E. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01428.x · Cited by 2,449 · see citing works
Hyldgaard, M., Mygind, T., & Meyer, R. L. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00012 · Cited by 2,191 · see citing works
Effect of essential oils on pathogenic bacteria
Nazzaro, F., Fratianni, F., De Martino, L., Coppola, R., & De Feo, V. (2013) · Pharmaceuticals · doi:10.3390/ph6121451 · Cited by 2,186 · see citing works
“It causes the release of LPS [13] and also acts on cytoplasmic membrane to alter the transport of ions.”
BackgroundResultInfluentialMechanisms of antibacterial action of three monoterpenes
Trombetta, D., Castelli, F., Sarpietro, M. G., Venuti, V., Cristani, M., Daniele, C., Saija, A., Mazzanti, G., & Bisignano, G. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.6.2474-2478.2005 · Cited by 1,359 · see citing works
Lactic Acid Permeabilizes Gram-Negative Bacteria by Disrupting the Outer Membrane
Alakomi, H.-L., Skyttä, E., Saarela, M., Mattila-Sandholm, T., Latva-Kala, K., & Helander, I. M. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.5.2001-2005.2000 · Cited by 1,093 · see citing works
Self-citationInvited review: essential oils as modifiers of rumen microbial fermentation
Calsamiglia, S., Busquet, M., Cardozo, P. W., Castillejos, L., & Ferret, A. (2007) · Journal of Dairy Science · doi:10.3168/jds.2006-644 · Cited by 1,014 · see citing works
Swamy, M. K., Akhtar, M. S., & Sinniah, U. R. (2016) · Evidence-Based Complementary and Alternative Medicine · doi:10.1155/2016/3012462 · Cited by 949 · see citing works
Application of natural antimicrobials for food preservation
Tiwari, B. K., Valdramidis, V. P., O’ Donnell, C. P., Muthukumarappan, K., Bourke, P., & Cullen, P. J. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf900668n · Cited by 851 · see citing works
Mechanisms of Action of Carvacrol on the Food-Borne Pathogen <i>Bacillus cereus</i>
Ultee, A., Kets, E. P. W., & Smid, E. J. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.10.4606-4610.1999 · Cited by 781 · see citing works
Self-citationCristani, M., D'Arrigo, M., Mandalari, G., Castelli, F., Sarpietro, M. G., Micieli, D., Venuti, V., Bisignano, G., Saija, A., & Trombetta, D. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf070094x · Cited by 671 · see citing works
Membrane toxicity of antimicrobial compounds from essential oils
Di Pasqua, R., Betts, G., Hoskins, N., Edwards, M., Ercolini, D., & Mauriello, G. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf0636465 · Cited by 648 · see citing works
The antibacterial mechanism of carvacrol and thymol against<i>Escherichia coli</i>
Xu, J., Zhou, F., Ji, B.-P., Pei, R.-S., & Xu, N. (2008) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2008.02407.x · Cited by 633 · see citing works
Zengin, H., & Baysal, A. (2014) · Molecules · doi:10.3390/molecules191117773 · Cited by 519 · see citing works
Antibacterial activity of leaf essential oils and their constituents from Cinnamomum osmophloeum
Chang, S.-T., Chen, P.-F., & Chang, S.-C. (2001) · Journal of Ethnopharmacology · doi:10.1016/s0378-8741(01)00273-2 · Cited by 514 · see citing works
Gill, A. O., & Holley, R. A. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.10.5750-5755.2004 · Cited by 439 · see citing works
Manipulation of rumen fermentation and methane production with plant secondary metabolites
Bodas, R., Prieto, N., García-González, R., Andrés, S., Giráldez, F. J., & López, S. (2012) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2012.07.010 · Cited by 437 · see citing works
Aromatic plants as a source of bioactive compounds
Christaki, E., Bonos, E., Giannenas, I., & Florou-Paneri, P. (2012) · Agriculture · doi:10.3390/agriculture2030228 · Cited by 346 · see citing works
Oussalah, M., Caillet, S., Saucier, L., & Lacroix, M. (2006) · Meat Science · doi:10.1016/j.meatsci.2005.11.019 · Cited by 307 · see citing works
Burt, S. A., van der Zee, R., Koets, A. P., de Graaff, A. M., van Knapen, F., Gaastra, W., Haagsman, H. P., & Veldhuizen, E. J. A. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00340-07 · Cited by 280 · see citing works
Exploring phytochemicals for combating antibiotic resistance in microbial pathogens
Khare, T., Anand, U., Dey, A., Assaraf, Y. G., Chen, Z.-S., Liu, Z., & Kumar, V. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.720726 · Cited by 281 · see citing works
Inhibition of bacterial cell division protein FtsZ by cinnamaldehyde
Domadia, P., Swarup, S., Bhunia, A., Sivaraman, J., & Dasgupta, D. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.06.029 · Cited by 276 · see citing works
Turgis, M., Han, J., Caillet, S., & Lacroix, M. (2009) · Food Control · doi:10.1016/j.foodcont.2009.02.001 · Cited by 236 · see citing works
IBRAHIM, M. A., KAINULAINEN, P., & AFLATUNI, A. (2001) · Agricultural and Food Science · doi:10.23986/afsci.5697 · Cited by 230 · see citing works
“Chanegriha et al. (1994) reported that, limonene and terpenyl acetate both inhibited the activity of B.”
BackgroundOlasupo, N. A., Fitzgerald, D. J., Gasson, M. J., & Narbad, A. (2003) · Letters in Applied Microbiology · doi:10.1046/j.1472-765x.2003.01427.x · Cited by 218 · see citing works
Paul, S., Dubey, R. C., Maheswari, D. K., & Kang, S. C. (2011) · Food Control · doi:10.1016/j.foodcont.2010.11.003 · Cited by 196 · see citing works
The effect of feeding essential oils on broiler performance and gut microbiota
Tiihonen, K., Kettunen, H., Bento, M. H. L., Saarinen, M., Lahtinen, S., Ouwehand, A. C., Schulze, H., & Rautonen, N. (2010) · British Poultry Science · doi:10.1080/00071668.2010.496446 · Cited by 186 · see citing works
Sharifi-Rad, J., Dey, A., Koirala, N., Shaheen, S., El Omari, N., Salehi, B., Goloshvili, T., Cirone Silva, N. C., Bouyahya, A., Vitalini, S., et al. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.600139 · Cited by 183 · see citing works
Potential application of spice and herb extracts as natural preservatives in cheese
Shan, B., Cai, Y.-Z., Brooks, J. D., & Corke, H. (2011) · Journal of Medicinal Food · doi:10.1089/jmf.2010.0009 · Cited by 168 · see citing works
Bacteriocidal effects and inhibition of cell separation of cinnamic aldehyde on Bacillus cereus
Kwon, J. A., Yu, C. B., & Park, H. D. (2003) · Letters in Applied Microbiology · doi:10.1046/j.1472-765x.2003.01350.x · Cited by 118 · see citing works
In vitro activity of carvacrol against staphylococcal preformed biofilm by liquid and vapour contact
Nostro, A., Marino, A., Blanco, A. R., Cellini, L., Di Giulio, M., Pizzimenti, F., Roccaro, A. S., & Bisignano, G. (2009) · Journal of Medical Microbiology · doi:10.1099/jmm.0.009274-0 · Cited by 99 · see citing works
Antiaflatoxigenic and antioxidant activity of an essential oil from <i>Ageratum conyzoides</i> L.
Patil, R. P., Nimbalkar, M. S., Jadhav, U. U., Dawkar, V. V., & Govindwar, S. P. (2010) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.3857 · Cited by 59 · see citing works
Effects of oregano essential oil on the ruminal pH and microbial population of sheep
Zhou, R., Wu, J., Zhang, L., Liu, L., Casper, D. P., Jiao, T., Liu, T., Wang, J., Lang, X., Song, S., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0217054 · Cited by 56 · see citing works
Chaichi, M., Mohammadi, A., Badii, F., & Hashemi, M. (2021) · Biocatalysis and Agricultural Biotechnology · doi:10.1016/j.bcab.2021.101926 · Cited by 34 · see citing works
Caillet, S., & Lacroix, M. (2006) · Journal of Food Protection · doi:10.4315/0362-028x-69.12.2961 · Cited by 35 · see citing works
- Authors
- Helander, I. M., Alakomi, H.-L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., Gorris, L. G. M., & von Wright, A.
- Affiliations
- VTT Technical Research Centre of Finland (FI)
- VTT Biotechnology and Food Research, P.O. Box 1501, FIN-02044 VTT, Finland, and Agrotechnological Research Institute (ATO-DLO), Bornsesteeg 59, NL-6708 PD Wageningen, The Netherlands
- Venue
- Journal of Agricultural and Food Chemistry
- Publisher
- American Chemical Society (ACS)
- Published
- 1998-08-11
- Volume
- 46
- Issue
- 9
- Pages
- 3590-3595
- ISSN
- 0021-8561 (ISSN-L)
- 1520-5118
- OpenAlex
- W2105402817
- Cited by
- 1,664
- References
- 22
- Citations by year
- 2026: 28 · 2025: 44 · 2024: 49 · 2023: 66 · 2022: 71 · 2021: 94 · 2020: 90 · 2019: 87 · 2018: 81 · 2017: 87 · 2016: 95 · 2015: 79 · 2014: 106 · 2013: 89 · 2012: 84
- FWCI
- 19.21
- Type
- journal article
- Language
- en
- Open access
- green
- research.wur.nl
- Locations
- Journal of Agricultural and Food Chemistry (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Essential Oils and Antimicrobial Activity
- Physical Sciences › Chemistry › Organic Chemistry › Antimicrobial agents and applications
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Insect Pest Control Strategies
- Keywords
- essential oil constituents, carvacrol, carvone, thymol, trans-cinnamaldehyde, antimicrobial activity, Escherichia coli O157:H7, Salmonella typhimurium, Photobacterium leiognathi, outer membrane disruption, lipopolysaccharide release, cytoplasmic membrane disruption, intracellular ATP, detergents, lysozyme
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