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 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.
Highlights
To survive starvation the Gram-positive bacterium Bacillus subtilis develops durable spores among other survival strategies [1]
Image analysis reveals drastic mother-cell volume loss To better understand the process of engulfment in the absence of the cell wall, we analyzed the volume and surface area of sporulating cells treated with cell-wall removal enzyme from previously published data [8]
In this work we presented image analysis and modeling of forespore engulfment in the absence of the cell wall
Summary
To survive starvation the Gram-positive bacterium Bacillus subtilis develops durable spores among other survival strategies [1]. Engulfment is successful in * 60 % of cells while the remaining * 40 % retract This observation raises questions on the origin of bistability and decision-making in relatively simple systems under severe energy limitations. Sporulation is initiated by asymmetric cell division after which the larger mother cell engulfs the smaller forespore, followed by spore maturation and release. This survival strategy is so robust that engulfment even proceeds when cells are deprived of their protective cell wall. We find physical parameter regimes responsible for bistable engulfment, including the number of bonds necessary for threshold-like engulfment and suitable osmotic pressures The former prediction matches previously published data, while we successfully tested the latter with time-lapse microscopy. Forespore engulfment in the absence of the cell wall is an ideal system to study phagocytosis-like processes and decision-making in single-cell organisms
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