The Phenolic Hydroxyl Group of Carvacrol Is Essential for Action against the Food-Borne Pathogen Bacillus cereus
Open accessAbstract
The natural antimicrobial compound carvacrol shows a high preference for hydrophobic phases. The partition coefficients of carvacrol in both octanol-water and liposome-buffer phases were determined (3.64 and 3.26, respectively). Addition of carvacrol to a liposomal suspension resulted in an expansion of the liposomal membrane. Maximum expansion was observed after the addition of 0.50 micromol of carvacrol/mg of L-alpha-phosphatidylethanolamine. Cymene, a biological precursor of carvacrol which lacks a hydroxyl group, was found to have a higher preference for liposomal membranes, thereby causing more expansion. The effect of cymene on the membrane potential was less pronounced than the effect of carvacrol. The pH gradient and ATP pools were not affected by cymene. Measurement of the antimicrobial activities of compounds similar to carvacrol (e.g., thymol, cymene, menthol, and carvacrol methyl ester) showed that the hydroxyl group of this compound and the presence of a system of delocalized electrons are important for the antimicrobial activity of carvacrol. Based on this study, we hypothesize that carvacrol destabilizes the cytoplasmic membrane and, in addition, acts as a proton exchanger, thereby reducing the pH gradient across the cytoplasmic membrane. The resulting collapse of the proton motive force and depletion of the ATP pool eventually lead to cell death.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Thymol has similar antimicrobial activity to carvacrol against B. cereus, S. aureus and P. aeruginosa, even though its hydroxyl group is located in a different position.
“Compared with carvacrol, thymol has similar antimicrobial activity against B. cereus, S. aureus and P. aeruginosa, even though its hydroxyl group is located in a different position [18,20].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [18]
Carvacrol is more effective than other essential oils, such as p-cymene.
“For example, carvacrol is more effective than other EOs, such as p-cymene [12,18,19].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [18]
p-Cymene can increase the antimicrobial activity of other compounds, such as its derivative carvacrol.
“p-cymene can also increase the antimicrobial activity of other compounds, such as its derivative carvacrol [18,23].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [18]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
Rouser, G., Fleischer, S., & Yamamoto, A. (1970) · Lipids · doi:10.1007/bf02531316 · Cited by 3,280 · 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
Interactions of cyclic hydrocarbons with biological membranes.
Sikkema, J., de Bont, J. A., & Poolman, B. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37154-5 · Cited by 1,203 · see citing works
An Introduction to Organic Chemistry
(1922) · Nature · doi:10.1038/109039d0 · Cited by 1,029 · 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
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-citationFluorescence method for measuring the kinetics of fusion between biological membranes
Hoekstra, D., Boer, T. D., Klappe, K., et al. (1984) · Biochemistry · doi:10.1021/bi00319a002 · Cited by 680 · 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
ANTIMICROBIAL EFFECTS OF SPICES1
Shelef, L. A. (1984) · Journal of Food Safety · doi:10.1111/j.1745-4565.1984.tb00477.x · Cited by 540 · see citing works
Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes
Weber, F. J., & de Bont, J. A. M. (1996) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/s0304-4157(96)00010-x · Cited by 515 · see citing works
Antimicrobial Activity of Carvacrol toward Bacillus cereus on Rice
Ultee, A., Slump, R. A., Steging, G., & Smid, E. J. (2000) · Journal of Food Protection · doi:10.4315/0362-028x-63.5.620 · Cited by 350 · see citing works
Self-citationBanerjee, S., Yalkowsky, S. H., & Valvani, C. (1980) · Environmental Science & Technology · doi:10.1021/es60170a013 · Cited by 318 · see citing works
Adaptation of the food-borne pathogen Bacillus cereus to carvacrol
Ultee, A., Kets, E. P. W., Alberda, M., Hoekstra, F. A., & Smid, E. J. (2000) · Archives of Microbiology · doi:10.1007/s002030000199 · Cited by 298 · see citing works
Self-citationBreeuwer, P., Drocourt, J.-L., ROMBOUTS, F. M., et al. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.1.178-183.1996 · Cited by 262 · see citing works
Effects of beta-pinene on yeast membrane functions
Uribe, S., Ramirez, J., & Peña, A. (1985) · Journal of Bacteriology · doi:10.1128/jb.161.3.1195-1200.1985 · Cited by 255 · see citing works
Composition and antioxidant activity of essential oils from Oregano plants grown wild in Greece
Lagouri, V., Blekas, G., Tsimidou, M. Z., Kokkini, S., & Boskou, D. G. (1993) · European Food Research and Technology · doi:10.1007/bf01202694 · Cited by 243 · see citing works
Solute partitioning into lipid bilayer membranes
Young, L. R. D., & Dill, K. A. (1988) · Biochemistry · doi:10.1021/bi00414a050 · Cited by 224 · see citing works
Bactericidal activity of carvacrol towards the food-borne pathogen Bacillus cereus
Ultee, Gorris, L. G. M., & Smid (1998) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1998.00467.x · Cited by 217 · see citing works
Vermuë, M. H., Sikkema, J., Verheul, A., Bakker, R., & TRAMPER, J. (1993) · Biotechnology and Bioengineering · doi:10.1002/bit.260420610 · Cited by 194 · see citing works
Mechanisms of membrane toxcity of hydrocarbons.
Sikkema, J., de Bont, J. A. M., & Poolman, B. (1995) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 178 · see citing works
Heipieper, H. J., Meulenbeld, G. H., van Oirschot, Q. E. A., & de Bont, J. A. M. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.8.2773-2777.1996 · Cited by 164 · see citing works
Ethanol dissipates the proton-motive force across the plasma membrane of Saccharomyces cerevisiae
Cartwright, C., juroszek, J., Beavan, M., et al. (1986) · Microbiology · doi:10.1099/00221287-132-2-369 · Cited by 154 · see citing works
Characteristics of self-quenching of the fluorescence of lipid-conjugated rhodamine in membranes.
MacDonald, R. I. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)77380-8 · Cited by 147 · see citing works
Spices and condiments: chemistry, microbiology, technology.
Pruthi, J. S. (1980) · PubMed · Cited by 131 · see citing works
Yield and composition of the essential oil of Thymus serpylloides subsp. serpylloides
Arrebola, M. L., Navarro, M., Jiménez, J., et al. (1994) · Phytochemistry · doi:10.1016/s0031-9422(00)97014-6 · Cited by 68 · see citing works
The hydrophobic expansion of erythrocyte membranes by the phenol anesthetics.
Machleidt, H., Roth, S., & Seeman, P. (1972) · Biochimica et Biophysica Acta · doi:10.1016/0005-2736(72)90020-x · Cited by 65 · see citing works
CHEMICAL SIGNIFICANCE OF THE VOLATILE COMPONENTS OF SPICES IN THE FOOD PRESERVATIVE VIEWPOINT-IV
KATAYAMA, T., & NAGAI, I. (1960) · NIPPON SUISAN GAKKAISHI · doi:10.2331/suisan.26.29 · Cited by 40 · see citing works
Action des acides hydroxycinnamiques libres et estérifiés sur la croissance des bactéries lactiques
Salih, A. G., Quéré, J. L., & Drilleau, J.-F. (2000) · Sciences des Aliments · doi:10.3166/sda.20.537-560 · Cited by 26 · see citing works
Katayama, T., & Nagai, I. (1960) · Cited by 25 · see citing works
Kıvanç, M., & Akgäul, A. (1988) · Flavour and Fragrance Journal · doi:10.1002/ffj.2730030209 · Cited by 21 · see citing works
ANTIMICROBIAL AND CYTOTOXIC ACTIVITIES OF OREGANUM ESSENTIAL OILS
Sivropoulou, A., Papinkolaou, E., & Nikolaou, C. (1996) · Cited by 18 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [6]6. Conner, D. E. 1993. Naturally occurring compounds, p. 441-468. In P. M. Davidson and A. L. Branen (ed.), Antimicrobials in foods, 2nd ed. Marcel Dekker, Inc., New York, N.Y.
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
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
Invited 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
Biological Activities of Essential Oils: From Plant Chemoecology to Traditional Healing Systems
Sharifi-Rad, J., Sureda, A., Tenore, G., Daglia, M., Sharifi-Rad, M., Valussi, M., Tundis, R., Sharifi-Rad, M., Loizzo, M., Ademiluyi, A., et al. (2017) · Molecules · doi:10.3390/molecules22010070 · Cited by 889 · 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
Antimicrobial activity of carvacrol related to its chemical structure
Ben Arfa, A., Combes, S., Preziosi-Belloy, L., Gontard, N., & Chalier, P. (2006) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2006.01938.x · Cited by 647 · 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
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
Patra, A. K., & Yu, Z. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.00309-12 · Cited by 416 · see citing works
Bhatta, R., Uyeno, Y., Tajima, K., Takenaka, A., Yabumoto, Y., Nonaka, I., Enishi, O., & Kurihara, M. (2009) · Journal of Dairy Science · doi:10.3168/jds.2008-1441 · Cited by 359 · see citing works
Kamatou, G. P. P., & Viljoen, A. M. (2010) · Journal of the American Oil Chemists Society · doi:10.1007/s11746-009-1483-3 · Cited by 357 · see citing works
Tao, N., Jia, L., & Zhou, H. (2014) · Food Chemistry · doi:10.1016/j.foodchem.2013.12.070 · Cited by 293 · 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
Effect of plant extracts on the techno-functional properties of biodegradable packaging films
Mir, S. A., Dar, B. N., Wani, A. A., & Shah, M. A. (2018) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2018.08.004 · Cited by 270 · see citing works
Essential oils as multicomponent mixtures and their potential for human health and well-being
Bunse, M., Daniels, R., Gründemann, C., Heilmann, J., Kammerer, D. R., Keusgen, M., Lindequist, U., Melzig, M. F., Morlock, G. E., Schulz, H., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.956541 · Cited by 210 · 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
Rattanachaikunsopon, P., & Phumkhachorn, P. (2010) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2010.06.010 · Cited by 152 · see citing works
Zhou, R., Wu, J., Lang, X., Liu, L., Casper, D. P., Wang, C., Zhang, L., & Wei, S. (2020) · Journal of Dairy Science · doi:10.3168/jds.2019-16611 · Cited by 130 · 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
Rajaei, A., Hadian, M., Mohsenifar, A., Rahmani-Cherati, T., & Tabatabaei, M. (2017) · Food Packaging and Shelf Life · doi:10.1016/j.fpsl.2017.10.005 · Cited by 85 · see citing works
Poudel, P., Froehlich, K., Casper, D. P., & St-Pierre, B. (2019) · Microorganisms · doi:10.3390/microorganisms7050120 · Cited by 58 · see citing works
Mousavi Khaneghah, A., Hashemi, S. M. B., Eş, I., Fracassetti, D., & Limbo, S. (2018) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-17-509 · Cited by 58 · 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
Seidi Damyeh, M., & Niakousari, M. (2017) · Industrial Crops and Products · doi:10.1016/j.indcrop.2017.01.029 · Cited by 41 · see citing works
Suwanamornlert, P., Sangchote, S., Chinsirikul, W., Sane, A., & Chonhenchob, V. (2018) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2018.02.009 · Cited by 41 · see citing works
Inactivation of Gram-positive bacteria by novel phenolic branched-chain fatty acids
Fan, X., Wagner, K., Sokorai, K. J. B., & Ngo, H. (2017) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-16-080 · Cited by 21 · see citing works
- Authors
- Ultee, A., Bennik, M. H. J., & Moezelaar, R.
- Affiliations
- Wageningen University & Research (NL)
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2002-04
- Volume
- 68
- Issue
- 4
- Pages
- 1561-1568
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC123826
- OpenAlex
- W2105644826
- Cited by
- 1,602
- References
- 32
- Citations by year
- 2026: 62 · 2025: 68 · 2024: 82 · 2023: 90 · 2022: 89 · 2021: 117 · 2020: 97 · 2019: 106 · 2018: 98 · 2017: 81 · 2016: 84 · 2015: 68 · 2014: 96 · 2013: 79 · 2012: 78
- FWCI
- 25.45
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- 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 › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
- Keywords
- carvacrol, cymene, Bacillus cereus, antimicrobial activity, phenolic hydroxyl groups, membrane permeabilization, proton motive force, ATP depletion, thymol, menthol, foodborne pathogens, hydrophobicity
- MeSH terms
- Cymenes, Adenosine Triphosphate, Anti-Bacterial Agents, Bacillus cereus, Cell Membrane, Food Microbiology, Hydrogen-Ion Concentration, Liposomes, Membrane Potentials, Microbial Sensitivity Tests, Phenols, Terpenes, Monoterpenes, Hydrophobic and Hydrophilic Interactions
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
