Intracellular Positioning Systems Limit the Entropic Eviction of Secondary Replicons Toward the Nucleoid Edges in Bacterial Cells. Issue 3 (7th February 2020)

• Record Type: Journal Article
• Authors: Planchenault, Charlène; Pons, Marine C.; Schiavon, Caroline; Siguier, Patricia; Rech, Jérôme; Guynet, Catherine; Dauverd–Girault, Julie; Cury, Jean; Rocha, Eduardo P.C.; Junier, Ivan; Cornet, François; Espéli, Olivier
• Is Part Of: Journal of molecular biology. Volume 432:Issue 3(2020)
• Page Start: 745
• Page End: 761
• Publication Date: 2020-02-07
• Subjects: plasmid -- chromosome -- partition -- segregation -- polymer unmixing; Molecular biology -- Periodicals; Biology -- Periodicals; Biochemistry -- Periodicals; Bacteriology -- Periodicals; Molecular Biology -- Periodicals; Biochemistry -- Periodicals; Biologie moléculaire -- Périodiques; Biologie -- Périodiques; Biochimie -- Périodiques; Moleculaire biologie; Biochemistry; Biology; Molecular biology; Periodicals; 572.805
• DOI: 10.1016/j.jmb.2019.11.027
• Languages: English
• ISSNs: 0022-2836

Abstract

Abstract: Bacterial genomes, organized intracellularly as nucleoids, are composed of the main chromosome coexisting with different types of secondary replicons. Secondary replicons are major drivers of bacterial adaptation by gene exchange. They are highly diverse in type and size, ranging from less than 2 to more than 1000 kb, and must integrate with bacterial physiology, including to the nucleoid dynamics, to limit detrimental costs leading to their counter-selection. We show that large DNA circles, whether from a natural plasmid or excised from the chromosome tend to localize in a dynamic manner in a zone separating the nucleoid from the cytoplasm at the edge of the nucleoid. This localization is in good agreement with silico simulations of DNA circles in the nucleoid volume. Subcellular positioning systems counteract this tendency, allowing replicons to enter the nucleoid space. In enterobacteria, these systems are found in replicons above 25 kb, defining the limit with small randomly segregated plasmids. Larger replicons carry at least one of the three described family of systems, ParAB, ParRM, and StbA. Replicons above 180 kb all carry a ParAB system, suggesting this system is specifically required in the cases of large replicons. Simulations demonstrated that replicon size profoundly affects localization, compaction, and dynamics of DNA circles in the nucleoid volume. The present work suggests that presence of partition systems on the larger plasmids or chromids is not only due to selection for accurate segregation but also to counteract their unmixing with the chromosome and consequent exclusion from the nucleoid. Graphical abstract: Image 1 Highlights: Secondary replicons above 25 kb always encode at least on partition system. The ParAB partition system serves as positioning system to maintain large replicon within nucleoid. DNA plasmid lacking partitioning system localized to the edge of the nucleoid. Positioning at the nucleoid edge is akin to polymer unmixing observed in simulations.