Single-Cell Division Triggers Immediate Efflux Phenotypic Switching to Environmental Toxins in Escherichia coli

Microbial communities in natural environments are consistently challenged by toxic compounds, such as polycyclic aromatic hydrocarbons (PAHs). The capacity for rapid phenotypic diversification is key to survival in these dynamic and often hostile niches. Here, we report a mechanism by which Escherichia coli (E. coli) generates immediate phenotypic heterogeneity in response to a model PAH, perylene. Utilising single-cell techniques, we revealed unexpected efflux phenotypic switches occurring in a single division event by examining the asymmetric distribution of perylene, a TolC-related efflux system substrate. Contrary to gradual changes in many generations, the phenotypic switch we observed is abrupt, resulting in daughter cells with distinct efflux phenotypes and asymmetric viability. We ruled out uneven efflux pump distribution and suggested the switch is linked to asymmetric proton motive force. Furthermore, we found a correlation between the age of the inherited pole during division and the propensity for phenotypic switching. New pole cells are identified as more prone to this switch. Our findings reveal a rapid division-based strategy for generating phenotypic diversity that could enhance the adaptive potential and resilience of bacterial populations facing fluctuating environmental toxins.