Phenotypic memory in Bacillus subtilis links dormancy entry and exit by a spore quantity-quality tradeoff

Abstract

Some bacteria, such as Bacillus subtilis, withstand starvation by forming dormant spores that revive when nutrients become available. Although sporulation and spore revival jointly determine survival in fluctuating environments, the relationship between them has been unclear. Here we show that these two processes are linked by a phenotypic “memory” that arises from a carry-over of molecules from the vegetative cell into the spore. By imaging life histories of individual B. subtilis cells using fluorescent reporters, we demonstrate that sporulation timing controls nutrient-induced spore revival. Alanine dehydrogenase contributes to spore memory and controls alanine-induced outgrowth, thereby coupling a spore’s revival capacity to the gene expression and growth history of its progenitors. A theoretical analysis, and experiments with signaling mutants exhibiting altered sporulation timing, support the hypothesis that such an intrinsically generated memory leads to a tradeoff between spore quantity and spore quality, which could drive the emergence of complex microbial traits.

Abstract

Bacillus subtilis withstands starvation by forming dormant spores that revive when nutrients become available. Here, Mutlu et al. show that sporulation timing controls spore revival through a phenotypic ‘memory’ that arises from the carry-over of a metabolic enzyme from the vegetative cell into the spore.