Bursting out: linking changes in nanotopography and biomechanical properties of biofilm-forming Escherichia coli to the T4 lytic cycle

The bacteriophage infection cycle has been extensively studied, yet little is known about the nanostructure and mechanical changes that lead to bacterial lysis. Here, atomic force microscopy was used to study in real time and in situ the impact of the canonical phage T4 on the nanotopography and biomechanics of irreversibly attached, biofilm-forming E. coli cells. The results show that in contrast to the lytic cycle in planktonic cells, which ends explosively, anchored cells that are in the process of forming a biofilm undergo a more gradual lysis, developing distinct nanoscale lesions (similar to 300nm in diameter) within the cell envelope. Furthermore, it is shown that the envelope rigidity and cell elasticity decrease (>50% and >40%, respectively) following T4 infection, a process likely linked to changes in the nanostructure of infected cells. These insights show that the well-established lytic pathway of planktonic cells may be significantly different from that of biofilm-forming cells. Elucidating the lysis paradigm of these cells may advance biofilm removal and phage therapeutics.

Automated summary

This study used atomic force microscopy to investigate the impact of phage T4 on the nanotopography and biomechanics of biofilm-forming E. coli cells. The results revealed that anchored cells undergoing biofilm formation experience a more gradual lysis with distinct nanoscale lesions, unlike the explosive lysis seen in planktonic cells. Furthermore, envelope rigidity and cell elasticity decrease significantly following T4 infection, indicating potential changes in the nanostructure of infected cells.