The Evolution of Mass Cell Suicide in Bacterial Warfare

Abstract

SUMMARYBehaviours that reliably cause the death of an actor are typically strongly disfavoured by natural selection, and yet many bacteria undergo cell lysis to release anti-competitor toxins [1–4]. This behaviour is most easily explained if only a few cells die to release toxins and help their clonemates, but the number of cells that actually lyse during bacterial warfare is unknown. The challenge is that one cannot distinguish cells that have undergone programmed suicide from those that were simply killed by a competitor’s toxin. We developed a two-colour fluorescence reporter assay in Escherichia coli to overcome this problem. Surprisingly, this revealed conditions where nearly all cells undergo programmed lysis. Adding a DNA-damaging toxin (DNase colicin) to a focal strain causes it to engage in mass cell suicide where around 85% of cells lyse to release their own toxin. Time-lapse 3D confocal microscopy revealed that self-lysis occurs at even higher frequencies (~94%) at the interface between competing colonies. We sought to understand how such high levels of cell suicide could be favoured by natural selection. Exposing E. coli that do not perform lysis to the DNase colicin revealed that mass lysis only occurs when cells are going to die anyway from toxin exposure. From an evolutionary perspective, this renders the behaviour cost-free as these cells have zero reproductive potential. This explains how mass cell suicide can evolve, as any small benefit to surviving clonemates can lead to the strategy being favoured by natural selection. Our findings have strong parallels to the suicidal attacks of social insects [5–8], which are also performed by individuals with low reproductive potential, suggesting convergent evolution in these very different organisms.HIGHLIGHTSA novel assay can detect Escherichia coli undergoing cell suicide to release toxinsWe quantified the frequency of suicidal self-lysis during competitionsUnder some conditions, nearly all cells will self-lyse to release toxinsSelf-lysis makes evolutionary sense as cells will die anyway from competitors’ toxins