A conserved mechanism drives partition complex assembly on bacterial chromosomes and plasmids

• Published in: Molecular systems biology Vol. 14; no. 11; pp. e8516 - n/a
• Main Authors: Debaugny, Roxanne E, Sanchez, Aurore, Rech, Jérôme, Labourdette, Delphine, Dorignac, Jérôme, Geniet, Frédéric, Palmeri, John, Parmeggiani, Andrea, Boudsocq, François, Anton Leberre, Véronique, Walter, Jean‐Charles, Bouet, Jean‐Yves
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.11.2018; EMBO Press; John Wiley and Sons Inc; Springer Nature
• Subjects: Adenosine triphosphatase; Assembly; Bacteria; Bacterial Proteins - metabolism; Bacteriology; Binding; Biochemistry, Molecular Biology; Biological Physics; Chromosome Segregation; Chromosomes; Chromosomes, Bacterial - genetics; Chromosomes, Bacterial - physiology; Coding; Deoxyribonucleic acid; DNA; DNA segregation; E coli; EMBO13; EMBO23; EMBO33; Escherichia coli; F plasmid; Life Sciences; Mathematical models; Microbiology and Parasitology; Models, Theoretical; Nucleation; ParABS; Partitions; Physics; plasmid partition; Plasmids; Plasmids - genetics; Plasmids - physiology; Proteins; Robustness (mathematics); Stochastic Processes; Stochasticity; Systems Biology - methods; Transcription; Vibrio cholerae - metabolism; Vibrio cholerae - physiology; Waterborne diseases; DNA segregation; F plasmid; ParABS; plasmid partition; Escherichia coli
• ISSN: 1744-4292; 1744-4292
• DOI: 10.15252/msb.20188516

Chromosome and plasmid segregation in bacteria are mostly driven by ParAB S systems. These DNA partitioning machineries rely on large nucleoprotein complexes assembled on centromere sites ( parS ). However, the mechanism of how a few parS ‐bound ParB proteins nucleate the formation of highly concentrated ParB clusters remains unclear despite several proposed physico‐mathematical models. We discriminated between these different models by varying some key parameters in vivo using the F plasmid partition system. We found that “Nucleation & caging” is the only coherent model recapitulating in vivo data. We also showed that the stochastic self‐assembly of partition complexes (i) is a robust mechanism, (ii) does not directly involve ParA ATPase, (iii) results in a dynamic structure of discrete size independent of ParB concentration, and (iv) is not perturbed by active transcription but is by protein complexes. We refined the “Nucleation & caging” model and successfully applied it to the chromosomally encoded Par system of Vibrio cholerae , indicating that this stochastic self‐assembly mechanism is widely conserved from plasmids to chromosomes. Synopsis High‐resolution ChIP‐seq and physico‐mathematical modeling are used to analyze the in vivo ParB DNA‐binding profiles. The “Nucleation and caging” self‐assembly mechanism is widespread to ensure faithful bacterial DNA segregation by ParAB S systems. ParB S partition complexes are highly dynamic nucleoprotein complexes. The robust ParB DNA binding profiles derived by ChIP‐seq data are well‐described by the “Nucleation and caging” model. The size of the partition complex is invariant to intracellular variation in ParB levels. This self‐assembly mechanism is observed on Escherichia coli and V. cholerae chromosomes and on the F plasmid. Graphical Abstract High‐resolution ChIP‐seq and physico‐mathematical modeling are used to analyze the in vivo ParB DNA‐binding profiles. The “Nucleation and caging” self‐assembly mechanism is widespread to ensure faithful bacterial DNA segregation by ParAB S systems.