The antibacterial effect of Tanacetum argyrophyllum essential oil on kanamycin-resistant Escherichia coli by disruption of energy metabolism and proton fluxes

银叶菊精油通过干扰能量代谢和质子流对卡那霉素耐药性大肠杆菌发挥抗菌作用

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Abstract

The essential oil (EO) of Tanacetum argyrophyllum harvested from Armenian flora (2080 m above sea level), characterized by a eucalyptol-camphor chemotype, and was investigated for its antibacterial activity, particularly against antibiotic-resistant bacterial strains. Chemical profiling revealed eucalyptol (35.0%), camphor (24.0%), and camphene (17.0%) as major constituents, alongside several minor terpenoids. The EO exhibited notable inhibitory effects against both wild-type Escherichia coli K-12 and kanamycin-resistant E. coli pARG-25 strains, with minimal inhibitory concentrations (MICs) reaching 100 µL/mL. . The combined influence of the EO with kanamycin could be described as synergistic, as Fractional Inhibitory Concentration Index (FICI) is 0.54. In this case the 62.5 µL/mL concentration of EO reduces the antibiotic MIC value fourfold. The investigation of colony-forming ability of bacteria under the influence of T. argyrophyllum EO revealed a reduction in bacterial viability by 30%. The changes in growth kinetics were also observed for both strains, which was indicated by a prolonged lag phase, suggesting impairment of early adaptation mechanisms. Further studies revealed that EO treatment significantly suppressed proton fluxes and ATPase activity in both strains. Particularly, total and DCCD-sensitive ATPase activities decreased by 1.5-fold, indicating a deviation in proton motive force maintenance and energy metabolism. The antibiotic-resistant E. coli pARG-25 strain exhibited higher ATPase activity compared to the wild-type, suggesting an elevated energy demand linked to resistance plasmid carriage, which was also targeted by the EO. These findings highlight that T. argyrophyllum EO disrupts bacterial energy homeostasis, representing a promising strategy for combating antibiotic-resistant pathogens. Overall, the results support the potential use of T. argyrophyllum EO as a natural antimicrobial agent.

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