The emergence of antibiotic-resistant bacteria highlights the need for novel natural antimicrobial agents. This study aimed to evaluate the chemical composition, antimicrobial activity, and redox-modulatory effects of Tanacetum argyrophyllum essential oil (EO) against Escherichia coli wild-type (E. coli K12) and kanamycin-resistant (E. coli pARG-25) strains. EO extraction yielded 0.1% (v/w), with eucalyptol (35%), camphor (24%), and camphene (17%) as major constituents, thus defining a eucalyptol–camphor chemotype. The minimum inhibitory concentrations were 100 µL/mL for both strains. Biophysical analyses revealed that EO exposure delayed the decline in the extracellular oxidation-reduction potential (ORP) and altered the pH dynamics, thus reflecting interference with bacterial kinetics, metabolic activity, and organic acid production. Biochemical assays indicated strain-specific oxidative stress responses: malondialdehyde formation increased by ~50% in the resistant strain, accompanied by substantial upregulation of superoxide dismutase and catalase activities, whereas the wild-type strain showed moderate changes. These data suggest that T. argyrophyllum EO disrupts bacterial redox homeostasis, likely via the modulation of antioxidant defenses, thus resulting in reduced viability and enhanced oxidative stress in resistant cells.
The findings provide some influence modes into EO-mediated bacteriostatic effects and support its potential as a natural agent that targets kanamycin-resistant bacteria through redox-dependent pathways.
Citation: Lusine Margaryan, Silvard Tadevosyan, Karen Trchounian, Naira Sahakyan. Disruption of bacterial redox homeostasis by Tanacetum argyrophyllum essential oil in antibiotic-sensitive and resistant Escherichia coli[J]. AIMS Biophysics, 2026, 13(2): 189-203. doi: 10.3934/biophy.2026011
The emergence of antibiotic-resistant bacteria highlights the need for novel natural antimicrobial agents. This study aimed to evaluate the chemical composition, antimicrobial activity, and redox-modulatory effects of Tanacetum argyrophyllum essential oil (EO) against Escherichia coli wild-type (E. coli K12) and kanamycin-resistant (E. coli pARG-25) strains. EO extraction yielded 0.1% (v/w), with eucalyptol (35%), camphor (24%), and camphene (17%) as major constituents, thus defining a eucalyptol–camphor chemotype. The minimum inhibitory concentrations were 100 µL/mL for both strains. Biophysical analyses revealed that EO exposure delayed the decline in the extracellular oxidation-reduction potential (ORP) and altered the pH dynamics, thus reflecting interference with bacterial kinetics, metabolic activity, and organic acid production. Biochemical assays indicated strain-specific oxidative stress responses: malondialdehyde formation increased by ~50% in the resistant strain, accompanied by substantial upregulation of superoxide dismutase and catalase activities, whereas the wild-type strain showed moderate changes. These data suggest that T. argyrophyllum EO disrupts bacterial redox homeostasis, likely via the modulation of antioxidant defenses, thus resulting in reduced viability and enhanced oxidative stress in resistant cells.
The findings provide some influence modes into EO-mediated bacteriostatic effects and support its potential as a natural agent that targets kanamycin-resistant bacteria through redox-dependent pathways.
antioxidant index
antimicrobial resistance
bicinchoninic acid
2,2-diphenyl-1-picrylhydrazyl
Essential oil
Gas Chromatography Mass Spectrometry
glutathione peroxidase
High-performance liquid chromatography
malondialdehyde
minimum inhibitory concentration
National Institute of Standards and Technology
Oxidation–reduction potential
reactive oxygen species
Relative Retention Index
Standard deviation
Superoxide dismutase
Thiobarbituric Acid
Thiobarbituric Acid Reactive Substances
wild type
| [1] |
Moghrovyan A, Sahakyan N (2024) Antimicrobial activity and mechanisms of action of Origanum vulgare L. essential oil: effects on membrane-associated properties. AIMS Biophys 11: 508-526. https://www.aimspress.com/article/doi/10.3934/biophy.2024027
|
| [2] |
Sahakyan N (2023) Lamiaceae family plants: One of the potentially richest sources of antimicrobials. Pharm Chem J 57: 565-572. https://doi.org/10.1007/s11094-023-02921-1
|
| [3] | Falleh H (2025) Demystifying the power of essential oils: a review of their antibacterial properties and potential as natural food preservatives. EXCLI J 24: 828-850. https://doi.org/10.17179/excli2025-8439 |
| [4] |
Eruygur N, Taban Akça K, Üstün O, et al. (2022) In vitro antioxidant and enzyme inhibition activity of Tanacetum argyrophyllum (K. Koch) tzvelev var. argyrophyllum extract. Turk J Pharm Sci 19: 377-382. https://doi.org/10.4274/tjps.galenos.2021.96493
|
| [5] | Kumar Biradar S, Tyagi CK (2021) Immunomodulatory activity of alcoholic extracts of Tinospora cordifolia stem. Res J Pharmacogn Phytochem 13: 73-77. https://doi.org/10.52711/0975-4385.2021.00012 |
| [6] | Margaryan L, Tadevosyan S, Sahakyan A, et al. (2026) The antibacterial effect of Tanacetum argyrophyllum essential oil on kanamycin-resistant Escherichia coli by disruption of energy metabolism and proton fluxes. Sci Rep . in press.https://doi.org/10.1038/s41598-026-44036-z |
| [7] |
Rajashekar CB (2023) Dual role of plant phenolic compounds as antioxidants and prooxidants. Am J Plant Sci 14: 15-28. https://doi.org/10.4236/ajps.2023.141002
|
| [8] |
Tadevosyan S, Babayan A, Sahakyan N (2025) Antioxidant and antibiotic-modulatory potential of Teucrium polium ethanolic extract against genetically-modified antibiotic-resistant E. coli strains. Iran J Med Microbiol 19: 107-117. https://doi.org/10.30699/ijmm.19.2.107
|
| [9] | Babayan A, Sahakyan N (2025) Origanum vulgare ethanol extract modulates the activity of antioxidant enzymes. Biochem Mosc Suppl B Biomed Chem 19: 316-326. https://doi.org/10.1134/S1990750825600505 |
| [10] |
Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11: 443-454. https://doi.org/10.1038/nrmicro3032
|
| [11] |
Dwyer DJ, Belenky PA, Yang JH, et al. (2014) Antibiotics induce redox-related physiological alterations as part of their lethality. Proc Natl Acad Sci USA 111: E2100-E2109. https://doi.org/10.1073/pnas.1401876111
|
| [12] |
Van Acker H, Coenye T (2017) The role of reactive oxygen species in antibiotic-mediated killing of bacteria. Trends Microbiol 25: 456-466. https://doi.org/10.1016/j.tim.2016.12.008
|
| [13] |
Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94: 223-253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
|
| [14] |
Nazzaro F, Fratianni F, De Martino L, et al. (2013) Effect of essential oils on pathogenic bacteria. Pharmaceuticals 6: 1451-1474. https://doi.org/10.3390/ph6121451
|
| [15] |
Silverstein TP (2021) The proton in biochemistry: impacts on bioenergetics, biophysical chemistry, and bioorganic chemistry. Front Mol Biosci 8: 764099. https://doi.org/10.3389/fmolb.2021.764099
|
| [16] |
Chiang SM, Schellhorn HE (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys 525: 161-169. https://doi.org/10.1016/j.abb.2012.02.007
|
| [17] | Tadevosyan S, Grabska S, Grabski H, et al. (2025) Menthol disruptive effects on kanamycin-resistant Escherichia coli energy metabolism and ion fluxes. Biophys Rep 5: 100240. https://doi.org/10.1016/j.bpr.2025.100240 |
| [18] | Gelashvili G, Gelenidze D, Abuladze M, et al. (2026) Response of bacterial antioxidant system to plasma-activated water as a disinfectant. Water (Basel) 18: 509. https://doi.org/10.3390/w18040509 |
| [19] |
Avetisyan A, Markosian A, Petrosyan M, et al. (2017) Chemical composition and some biological activities of the essential oils from basil Ocimum different cultivars. BMC Complement Altern Med 17: 60. https://doi.org/10.1186/s12906-017-1587-5
|
| [20] |
Beauchamp C, Fridovich I (1970) A mechanism for the production of ethylene from methional. The generation of the hydroxyl radical by xanthine oxidase. J Biol Chem 245: 4641-4646. https://doi.org/10.1016/S0021-9258(18)62842-X
|
| [21] |
Ginovyan M, Gevorgyan S, Javrushyan H, et al. (2026) Inhibition of the PI3K signaling pathway in cancer cells by Agrimonia eupatoria L. ethanolic extract: identification of tricoumaroyl spermidine as a potential PI3K inhibitor. BMC Complement Med Ther 26: 41. https://doi.org/10.1186/s12906-025-05231-z
|
| [22] |
Petrosyan H, Trchounian K (2024) Growth characteristics, redox potential changes and proton motive force generation in Thermus scotoductus K1 during growth on various carbon sources. AIMS Microbiol 10: 1052-1067. https://doi.org/10.3934/microbiol.2024045
|
| [23] |
Akpulat HA, Tepe B, Sokmen A, et al. (2005) Composition of the essential oils of Tanacetum argyrophyllum (C. Koch) tvzel. var. argyrophyllum and tanacetum parthenium (L.) schultz bip. (Asteraceae) from Turkey. Biochem Syst Ecol 33: 511-516. https://doi.org/10.1016/J.BSE.2004.10.006
|
| [24] |
Prakash Bhanu, Dubey NK, Freitas Brilhante de São José Jackline (2024) Plant Essential Oils: From Traditional To Modern Day Application. Springer. https://doi.org/10.1007/978-981-99-4370-8
|
| [25] |
Aćimović M, Zeremski T, Šovljanski O, et al. (2022) Seasonal variations in essential oil composition of immortelle cultivated in Serbia. Horticulturae 8: 1183. https://doi.org/10.3390/horticulturae8121183
|
| [26] | Torres-Martínez R, García-Rodríguez YM, Ríos-Chávez P, et al. (2018) Antioxidant activity of the essential oil and its major terpenes of Satureja macrostema (moc. and sessé ex benth.) briq. Pharmacogn Mag 13: S875-S880. https://doi.org/10.4103/pm.pm_316_17 |
| [27] |
Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014: 1-31. https://doi.org/10.1155/2014/360438
|
| [28] |
Singh D (2022) Juggling with reactive oxygen species and antioxidant defense system – A coping mechanism under salt stress. Plant Stress 5: 100093. https://doi.org/10.1016/j.stress.2022.100093
|
| [29] |
Borisov VB, Siletsky SA, Nastasi MR, et al. (2021) ROS defense systems and terminal oxidases in bacteria. Antioxidants 10: 839. https://doi.org/10.3390/antiox10060839
|
| [30] | Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex J Med 54: 287-293. https://doi.org/10.1016/j.ajme.2017.09.001 |
| [31] |
Wang X, Zhao X (2009) Contribution of oxidative damage to antimicrobial; ethality. Antimicrob Agents Chemother 53: 1395-1402. https://doi.org/10.1128/AAC.01087-08
|
| [32] |
Peng B, Li H, Peng X (2025) Metabolic state-driven nutrient-based approach to combat bacterial antibiotic resistance. npj Antimicrobials Resist 3: 24. https://doi.org/10.1038/s44259-025-00092-5
|
| [33] | Krishnaiah D, Bono A, Sarbatly R, et al. (2007) Physiological responses of Escherichia coli cells cultivated under a sublethal oxidative stress condition. Malays J Microbiol 3: 14-18. https://doi.org/10.21161/mjm.05007 |