Compaction of bacterial genomic DNA: Clarifying the concepts

Abstract

The unconstrained genomic DNA of bacteria forms a coil, which volume exceeds 1000 times the volume of the cell. Since prokaryotes lack a membrane-bound nucleus, in sharp contrast with eukaryotes, the DNA may consequently be expected to occupy the whole available volume when constrained to fit in the cell. Still, it has been known for more than half a century that the DNA is localized in a well defined region of the cell, called the nucleoid, which occupies only 15% to 25% of the total volume. Although this problem has focused the attention of many scientists for the past decades, there is still no certainty concerning the mechanism that enables such a dramatic compaction. The goal of this Topical Review is to take stock of our knowledge on this question by listing all possible compaction mechanisms with the proclaimed desire to clarify the physical principles they are based upon and discuss them in the light of experimental results and the results of simulations based on coarse-grained models. In particular, the fundamental differences between psi-condensation and segregative phase separation and between the condensation by small and long polycations are highlighted. This review suggests that the importance of certain mechanisms, like supercoiling and the architectural properties of DNA-bridging and DNA-bending nucleoid proteins, may have been overestimated, whereas other mechanisms, like segregative phase separation and the self-association of nucleoid proteins, as well as the possible role of the synergy of two or more mechanisms, may conversely deserve more attention.

published as a Topical Review but contains also original research results

References in corpus (5)

• Description of non-specific DNA-protein interaction and facilitated diffusion with a dynamical model
• A model of H-NS mediated compaction of bacterial DNA
• Comparison of kinetic and dynamical models of DNA-protein interaction and facilitated diffusion
• Dynamical model of DNA-protein interaction: effect of protein charge distribution and mechanical properties
• Equilibration of complexes of DNA and H-NS proteins on charged surfaces: A coarse-grained model point of view

Cited by in corpus (18)

• DNA supercoiling in bacteria: state of play and challenges from a viewpoint of physics based modeling
• In vivo compaction dynamics of bacterial DNA: A fingerprint of DNA/RNA demixing ?
• Preferential localization of the bacterial nucleoid
• Bacterial nucleoid: Interplay of DNA demixing and supercoiling
• Organization of the bacterial nucleoid by DNA-bridging proteins and globular crowders
• Role of salt valency in the switch of H-NS proteins between DNA-bridging and DNA-stiffening modes
• Coarse-Grained model of the demixing of DNA and non-binding globular macromolecules
• Entropic elasticity and dynamics of the bacterial chromosome: a simulation study
• Impact of self-association on the architectural properties of bacterial nucleoid proteins
• Bacterial chromosome organization II: few special cross-links, cell confinement, and molecular crowders play the pivotal roles
• Requirements for DNA-bridging proteins to act as topological barriers of the bacterial genome
• Bacterial chromosome organization I: crucial role of release of topological constraints and molecular crowders
• Origin of spatial organization of DNA-polymer in bacterial chromosomes
• Topology mediated organization of E.coli chromosome in fast growth conditions
• Role of special cross-links in structure formation of bacterial DNA polymer
• Tethered Particle Motion Technique in Crowded Media: Compaction of DNA by Globular Macromolecules
• DNA-polymer architecture orchestrates the segregation and spatio-temporal organization of E. coli chromosomes during replication in slow growth
• A sheet-like structure in the proximity of compact DNA