Bistable forespore engulfment in Bacillus subtilis by a zipper mechanism in absence of the cell wall

TL;DR

This study investigates the biophysical mechanism behind bistable forespore engulfment in Bacillus subtilis, revealing how ligand-receptor interactions can drive rapid, cell-wall independent engulfment through a zipper-like process.

Contribution

The paper combines experimental imaging and stochastic simulations to elucidate how SpoIIQ-SpoIIIAH bonds enable bistable, cell-wall independent engulfment in bacteria.

Findings

Engulfment is sensitive to SpoIIQ-SpoIIIAH bond number.

Osmotic pressure and membrane tension influence successful engulfment.

Decreasing osmolarity experimentally prevents engulfment.

Abstract

To survive starvation, the bacterium Bacillus subtilis forms durable spores. The initial step of sporulation is asymmetric cell division, leading to a large mother-cell and a small forespore compartment. After division is completed and the dividing septum is thinned, the mother cell engulfs the forespore in a slow process based on cell-wall degradation and synthesis. However, recently a new cell-wall independent mechanism was shown to significantly contribute, which can even lead to fast engulfment in $\sim$ 60 $%$ of the cases when the cell wall is completely removed. In this backup mechanism, strong ligand-receptor binding between mother-cell protein SpoIIIAH and forespore-protein SpoIIQ leads to zipper-like engulfment, but quantitative understanding is missing. In our work, we combined fluorescence image analysis and stochastic Langevin simulations of the fluctuating membrane to investigate the origin of fast bistable engulfment in absence of the cell wall. Our cell morphologies compare favorably with experimental time-lapse microscopy, with engulfment sensitive to the number of SpoIIQ-SpoIIIAH bonds in a threshold-like manner. By systematic exploration of model parameters, we predict regions of osmotic pressure and membrane-surface tension that produce successful engulfment. Indeed, decreasing the medium osmolarity in experiments prevents engulfment in line with our predictions. Forespore engulfment may thus not only be an ideal model system to study decision-making in single cells, but its biophysical principles are likely applicable to engulfment in other cell types, e.g. during phagocytosis in eukaryotes.