A Type IV Pilus Mediates DNA Binding during Natural Transformation in Streptococcus pneumoniae

Raphaël Laurenceau,Rémi Fronzes,Jean-Pierre Claverys,Sonia Baconnais,Gérard Péhau-Arnaudet,Julia Chamot-Rooke,Annick Dujeancourt,Joseph Gault,Christian Malosse,Nathalie Campo,Eric Le Cam

doi:10.1371/journal.ppat.1003473

Abstract

Natural genetic transformation is widely distributed in bacteria and generally occurs during a genetically programmed differentiated state called competence. This process promotes genome plasticity and adaptability in Gram-negative and Gram-positive bacteria. Transformation requires the binding and internalization of exogenous DNA, the mechanisms of which are unclear. Here, we report the discovery of a transformation pilus at the surface of competent Streptococcus pneumoniae cells. This Type IV-like pilus, which is primarily composed of the ComGC pilin, is required for transformation. We provide evidence that it directly binds DNA and propose that the transformation pilus is the primary DNA receptor on the bacterial cell during transformation in S. pneumoniae. Being a central component of the transformation apparatus, the transformation pilus enables S. pneumoniae, a major Gram-positive human pathogen, to acquire resistance to antibiotics and to escape vaccines through the binding and incorporation of new genetic material.

Highlights

Natural transformation, first discovered in Streptococcus pneumoniae [1], is observed in many Gram-negative and Gram-positive bacteria [2]
We discovered a new appendage at the surface of S. pneumoniae cells
We show that this appendage is similar in morphology and composition to appendages called Type IV pili commonly found in Gram-negative bacteria

Summary

Introduction

First discovered in Streptococcus pneumoniae [1], is observed in many Gram-negative and Gram-positive bacteria [2] It increases bacterial adaptability by promoting genome plasticity through intra- and inter-species genetic exchange [3]. In S. pneumoniae, a major human pathogen responsible for severe diseases such as pneumonia, meningitis and septicemia, transformation is presumably responsible for capsular serotype switching and could reduce the efficiency of capsule-based vaccines after a short period [4]. In this species, it occurs during a genetically programmed and differentiated state called competence that is briefly induced at the beginning of exponential growth. In S. pneumoniae, some antibiotics and DNA-damaging agents induce competence, which would act as an alternative SOS response and increases bacterial resistance to external stresses [6]

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Conclusion