The alternative sigma factor σX mediates competence shut-off at the cell pole in Streptococcus pneumoniae

Calum HG Johnston,Marc Prudhomme,Patrice Polard,Matthieu Bergé,David De Lemos,Anne-Lise Soulet

doi:10.7554/elife.62907

Calum HG Johnston, Marc Prudhomme + Show 4 more

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https://doi.org/10.7554/elife.62907

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Abstract

Competence is a widespread bacterial differentiation program driving antibiotic resistance and virulence in many pathogens. Here, we studied the spatiotemporal localization dynamics of the key regulators that master the two intertwined and transient transcription waves defining competence in Streptococcus pneumoniae. The first wave relies on the stress-inducible phosphorelay between ComD and ComE proteins, and the second on the alternative sigma factor σX, which directs the expression of the DprA protein that turns off competence through interaction with phosphorylated ComE. We found that ComD, σX and DprA stably co-localize at one pole in competent cells, with σX physically conveying DprA next to ComD. Through this polar DprA targeting function, σX mediates the timely shut-off of the pneumococcal competence cycle, preserving cell fitness. Altogether, this study unveils an unprecedented role for a transcription σ factor in spatially coordinating the negative feedback loop of its own genetic circuit.

Highlights

In bacteria, sigma (σ) factors are essential transcription effectors that direct the RNA polymerase to and activate RNA synthesis at specific genes promoters
This study revealed that the entire pneumococcal competence cycle occurs at cell pole, from its induction triggered by ComD, ComE and CSP to its shut-off mediated by DprA and assisted by σX
DprA displays a polar localization in competent cells, which correlates with competence shut-off

Summary

Introduction

Sigma (σ) factors are essential transcription effectors that direct the RNA polymerase to and activate RNA synthesis at specific genes promoters. Many bacteria encode a variable set of alternative σ factors that control specific regulons, providing appropriate properties to the cells in response to various stimuli These alternative σ factors play pivotal roles in the multifaceted lifestyles of bacteria. They trigger specific developmental programs, such as sporulation or biofilm formation, as well as adapted responses to multiple types of stress and virulence in some pathogenic species (Kazmierczak et al., 2005). How these alternative σ factors are activated in the cell has been extensively studied, revealing multiple mechanisms underlying their finely tuned regulation(Österberg et al, 2011a). How these mechanisms are orchestrated spatiotemporally within the cell remains poorly understood

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