When starved, the Gram-positive bacterium Bacillus subtilis forms durable spores for survival. Sporulation initiates with an asymmetric cell division, creating a large mother cell and a small forespore. Subsequently, the mother cell membrane engulfs the forespore in a phagocytosis-like process. However, the force generation mechanism for forward membrane movement remains unknown. Here, we show that membrane migration is driven by cell wall remodeling at the leading edge of the engulfing membrane, with peptidoglycan synthesis and degradation mediated by penicillin binding proteins in the forespore and a cell wall degradation protein complex in the mother cell. We propose a simple model for engulfment in which the junction between the septum and the lateral cell wall moves around the forespore by a mechanism resembling the ‘template model’. Hence, we establish a biophysical mechanism for the creation of a force for engulfment based on the coordination between cell wall synthesis and degradation.
Some bacteria, such as Bacillus subtilis, form spores when starved of food, which enables them to lie dormant for years and wait for conditions to improve. To make a spore, the bacterial cell divides to make a larger mother cell and a smaller forespore cell. Then the membrane that surrounds the mother cell moves to surround the forespore and engulf it. For this process to take place, a rigid mesh-like layer called the cell wall, which lies outside the cell membrane, needs to be remodelled. This happens once a partition in the cell wall, called a septum, has formed, separating mother and daughter cells. However, it is not clear how the mother cell can generate the physical force required to engulf the forespore under the cramped conditions imposed by the cell wall.
To address this question, Ojkic, López-Garrido et al. used microscopy to investigate how B. subtilis makes spores. The experiments show that, in order to engulf the forespore, the mother cell must produce new cell wall and destroy cell wall that is no longer needed. Running a simple biophysical model on a computer showed that coordinating these two processes could generate enough force for a mother cell to engulf a forespore.
Ojkic, López-Garrido et al. propose that the junction between the septum and the cell wall moves around the forespore to make room for the mother cell’s membrane for expansion. Other spore-forming bacteria that threaten human health – such as Clostridium difficile, which causes bowel infections, and Bacillus anthracis, which causes anthrax – might form their spores in the same way, but this remains to be tested. More work will also be needed to understand exactly how bacterial cells coordinate the cell wall synthesis and cell wall degradation.