title: Pneumococcal Competence Coordination Relies on a Cell-Contact Sensing Mechanism.
abstract: Bacteria have evolved various inducible genetic programs to face many types of stress that challenge their growth and survival. Competence is one such program. It enables genetic transformation, a major horizontal gene transfer process. Competence development in liquid cultures of Streptococcus pneumoniae is synchronized within the whole cell population. This collective behavior is known to depend on an exported signaling Competence Stimulating Peptide (CSP), whose action generates a positive feedback loop. However, it is unclear how this CSP-dependent population switch is coordinated. By monitoring spontaneous competence development in real time during growth of four distinct pneumococcal lineages, we have found that competence shift in the population relies on a self-activated cell fraction that arises via a growth time-dependent mechanism. We demonstrate that CSP remains bound to cells during this event, and conclude that the rate of competence development corresponds to the propagation of competence by contact between activated and quiescent cells. We validated this two-step cell-contact sensing mechanism by measuring competence development during co-cultivation of strains with altered capacity to produce or respond to CSP. Finally, we found that the membrane protein ComD retains the CSP, limiting its free diffusion in the medium. We propose that competence initiator cells originate stochastically in response to stress, to form a distinct subpopulation that then transmits the CSP by cell-cell contact.
authors.affiliation: Laboratoire de Microbiologie et Génétique Moléculaires, Centre de Biologie Integrative, Université de Toulouse, CNRS, UPS, France.
authors.forename: Marc
authors.initials: M
authors.lastname: Prudhomme
authors.affiliation: Laboratoire de Microbiologie et Génétique Moléculaires, Centre de Biologie Integrative, Université de Toulouse, CNRS, UPS, France.
authors.forename: Mathieu
authors.initials: M
authors.lastname: Berge
authors.affiliation: Laboratoire de Microbiologie et Génétique Moléculaires, Centre de Biologie Integrative, Université de Toulouse, CNRS, UPS, France.
authors.forename: Bernard
authors.initials: B
authors.lastname: Martin
authors.affiliation: Laboratoire de Microbiologie et Génétique Moléculaires, Centre de Biologie Integrative, Université de Toulouse, CNRS, UPS, France.
authors.forename: Patrice
authors.initials: P
authors.lastname: Polard
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics*; D002450:Cell Communication / Q000235:genetics*; D061269:DNA Transformation Competence / Q000235:genetics*; D015964:Gene Expression Regulation, Bacterial / Q000235:genetics; D022761:Gene Transfer, Horizontal / Q000235:genetics; D005798:Genes, Bacterial / Q000235:genetics; D008565:Membrane Proteins / Q000235:genetics; D010455:Peptides / Q000235:genetics; D013296:Streptococcus pneumoniae / Q000235:genetics*
chemical_list: D001426:Bacterial Proteins; D008565:Membrane Proteins; D010455:Peptides; C423628:competence factor, Streptococcus