Metabolomics Study Reveals Enhanced Inhibition and Metabolic Dysregulation in Escherichia coli Induced by Lactobacillus acidophilus-Fermented Black Tea Extract

Abstract

This study examined the ability of Lactobacillus acidophilus (LA) to ferment black tea extract (BTE) and the enhancement of Escherichia coli cellular uptake of phenolic compounds when these bacteria were incubated with fermented BTE. The inhibitory effects of BTE to E. coli bacteria with and without fermentation were compared. Several intracellular phenolic compounds as well as metabolic profiles of E. coli with and without treatments were also determined using a high-performance liquid chromatography-tandem mass spectrometry-based approach. Our results showed that of three concentrations from the non-fermented BTE treatment, only the extract from the 25 mg/mL tea leaves solution could inhibit E. coli survival, while LA-fermented BTE extract from 5, 10, and 25 mg/mL tea leaves solutions all inhibited E. coli growth significantly. Intracellular concentrations of (+)-catechin-3-gallate/(-)-epicatechin-3-gallate and (+)-catechin/(-)-epicatechin were significantly higher when E. coli was treated with fermented BTE in comparison to non-fermented BTE. Scanning electron microscopy images indicated that the intracellular phenolic compounds inhibited E. coli growth by increasing endogenous oxidative stress. Metabolic profiles of E. coli were also investigated to understand their metabolic response when treated with BTE, and significant metabolic changes of E. coli were observed. Metabolic profile data were further analyzed using partial least squares discriminant analysis to distinguish the fermented BTE treatment group from the control group and the non-fermented BTE treatment group. The results indicated a large-scale E. coli metabolic dysregulation induced by the fermented BTE. Our findings showed that LA fermentation can be an efficient approach to enhance phenolic inhibition of bacterial cells through increased endogenous oxidative stress and dysregulated metabolic activities.