Abstract
BackgroundBacterial spores can remain dormant for decades, yet harbor the exceptional capacity to rapidly resume metabolic activity and recommence life. Although germinants and their corresponding receptors have been known for more than 30 years, the molecular events underlying this remarkable cellular transition from dormancy to full metabolic activity are only partially defined.ResultsHere, we examined whether protein phospho-modifications occur during germination, the first step of exiting dormancy, thereby facilitating spore revival. Utilizing Bacillus subtilis as a model organism, we performed phosphoproteomic analysis to define the Ser/Thr/Tyr phosphoproteome of a reviving spore. The phosphoproteome was found to chiefly comprise newly identified phosphorylation sites located within proteins involved in basic biological functions, such as transcription, translation, carbon metabolism, and spore-specific determinants. Quantitative comparison of dormant and germinating spore phosphoproteomes revealed phosphorylation dynamics, indicating that phospho-modifications could modulate protein activity during this cellular transition. Furthermore, by mutating select phosphorylation sites located within proteins representative of key biological processes, we established a functional connection between phosphorylation and the progression of spore revival.ConclusionsHerein, we provide, for the first time, a phosphoproteomic view of a germinating bacterial spore. We further show that the spore phosphoproteome is dynamic and present evidence that phosphorylation events play an integral role in facilitating spore revival.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0184-7) contains supplementary material, which is available to authorized users.
Highlights
Bacterial spores can remain dormant for decades, yet harbor the exceptional capacity to rapidly resume metabolic activity and recommence life
The revival process has been classically divided into two major consecutive phases: (1) germination, in which nutrients bind to germinant receptors located in the spore inner membrane, triggering the release of monovalent cations (H+, K+) and Dipicolinic acid (DPA), spore rehydration, cortex hydrolysis, and coat disassembly; we have recently shown that the completion of this process requires active translation [15]
The phosphoproteome of a reviving spore is dynamic and spans key biological processes To explore whether spore revival involves phosphorylation events in spore proteins, we sought to characterize the phosphoproteome of a germinating spore
Summary
Bacterial spores can remain dormant for decades, yet harbor the exceptional capacity to rapidly resume metabolic activity and recommence life. Germinants and their corresponding receptors have been known for more than 30 years, the molecular events underlying this remarkable cellular transition from dormancy to full metabolic activity are only partially defined. In response to nutrient deprivation, bacteria of various Bacillus species can carry out a complex developmental process called sporulation, resulting in the formation of a highly durable spore, the most resilient cell type known. The core is protected from the environment by a relatively impermeable inner membrane, which in turn is encased by a thick peptidoglycan layer, called a cortex. The chromosome, the most vital molecular constituent within the spore core, is protected by specialized spore-specific DNA binding
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