Chromosomal organization governs the timing of cell type-specific gene expression required for spore formation in Bacillus subtilis

Abstract

During the early stages of spore formation in Bacillus subtilis, asymmetric division precedes chromosome segregation, such that the forespore transiently contains only about one-third of the genetic material surrounding the origin of replication. Shortly after septum formation, the transcription factor σF initiates forespore-specific gene expression that is essential for the proteolytic activation of pro-σE in the neighbouring mother cell. Moving the σF-dependent spollR gene from its original origin-proximal position to an ectopic origin-distal site caused a delay in spollR transcription, as well as delays and reductions in the proteolytic activation of pro-σE and σE-directed gene expression. These defects correlated with the accumulation of disporic sporangia, thus reducing sporulation efficiency in a manner that depended upon the distance that spollR had been moved from the origin-proximal third of the chromosome. A significant proportion of disporic sporangia exhibited σE activity in their central compartment, indicating that delays and reductions in σE activation can lead to the formation of a second septum at the opposite pole. These observations support a model in which chromosomal spollR position temporally regulates σE activation, thereby allowing for the rapid establishment of mother cell-specific gene expression that is essential for efficient spore formation. The implications of these findings for cell type-specific gene expression during the early stages of spore formation in B. subtilis are discussed.