Surfing on Protein Waves: Proteophoresis as a Mechanism for Bacterial Genome Partitioning

Abstract

Efficient bacterial chromosome segregation typically requires the coordinated action of a threecomponent, fueled by adenosine triphosphate machinery called the partition complex. We present a phenomenological model accounting for the dynamic activity of this system that is also relevant for the physics of catalytic particles in active environments. The model is obtained by coupling simple linear reaction-diffusion equations with a proteophoresis, or "volumetric" chemophoresis, force field that arises from protein-protein interactions and provides a physically viable mechanism for complex translocation. This minimal description captures most known experimental observations: dynamic oscillations of complex components, complex separation and subsequent symmetrical positioning. The predictions of our model are in phenomenological agreement with and provide substantial insight into recent experiments. From a non-linear physics view point, this system explores the active separation of matter at micrometric scales with a dynamical instability between static positioning and travelling wave regimes triggered by the dynamical spontaneous breaking of rotational symmetry.Controlled motion and positioning of colloids and macromolecular complexes in a fluid, as well as catalytic particles in active environments, are fundamental processes in physics, chemistry and biology with important implications for technological applications [1,2]. In this paper, we focus on an active biological system for which precise experimental results are available. Our work is fully inspired by studies of one of the most widespread and ancient mechanisms of liquid phase macromolecular segregation and positioning known in nature: bacterial DNA segregation systems. Despite the fundamental importance of these systems in the bacterial world and intensive experimental studies extending over 30-years [3-5], no global picture encompasses fully the experimental observations. Partition systems encode only three elements that are necessary and sufficient for active partitioning: two proteins ParA and ParB, and a specific sequence parS encoded on DNA. The pool of ParB proteins is recruited as a cluster of spherical shape centered around the sequence parS, forming the ParBS partition complex [4]. These ParBS cargos interact with ParA bound onto chromosomal DNA (ParA-slow) [6,7], triggering unbinding of ParA by inducing conformational changes through stimulation of adenosine triphosphate (ATP) hydrolysis and/or direct ParB-ParA contact [8], and thereby allowing ParA diffusion in the cytoplasm (ParA-fast) [5]. This process entails the oscillation of ParA from pole to pole and the separation of the ParBS partition complex into two complexes with distinct sub-cellular trajectories and long-term localization. Overall, these interactions result in an equidistant, stable positioning of the duplicated DNA molecules along the cell axis.The specific modeling of ParABS systems falls into two categories: either "filament" (pushing/pulling the cargos, similar to eukaryotic...

Looping and clustering model for the organization of protein-DNA complexes on the bacterial genome

“…A central component of this system is the partitioning module, which is formed by a large protein-DNA complex of ParB proteins that assembles around centromere-like parS sites, frequently located near the origin of replication. The ParBS complexes can subsequently interact with ParA ATPases, leading to the segregation of replicated origins [18][19][20][21][22][23][24][25]. How is this ParBS partitioning module physically organized on the DNA?…”

Center Finding in E. coli and the Role of Mathematical Modeling: Past, Present and Future

“…However, we emphasise that there are still many similarities between the two systems. Plasmid systems are also capable, at least theoretically, of displaying oscillations [56,58,59] and both are examples of mass-conserving patterning dynamics. A related system, PomXYZ of Myxococcus xanthus, sits between the two.…”

Robust and conserved stochastic self-assembly mechanism for dynamic ParB-parSpartition complexes on bacterial chromosomes and plasmids

“…ParA-driven mechanism that ensures the proper location and the directed segregation of replicons relies on the positioning of ParBS partition complexes within the nucleoid volume (Le Gall et al, 2016) and on a reaction diffusion-based mechanism (Hu et al, 2017;Hwang et al, 2013;Lim et al, 2014;Walter et al, 2017).…”