The PomXYZ Proteins Self-Organize on the Bacterial Nucleoid to Stimulate Cell Division

Schumacher, Dominik; Bergeler, Silke; Harms, Andrea; Vonck, Janet; Huneke-Vogt, Sabrina; Frey, Erwin; Søgaard‐Andersen, Lotte

doi:10.1016/j.devcel.2017.04.011

Cited by 69 publications

(163 citation statements)

References 67 publications

Supporting

Mentioning

150

Contrasting

Order By: Relevance

“…The placement of the Z-ring has been shown to be regulated by proteins belonging to the ParA-like family of Walker-type ATPases in many organisms such as Escherichia coli (de Boer et al, 1989;Raskin and de Boer, 1999), Bacillus subtilis (Marston et al, 1998), Caulobacter crescentus (Thanbichler and Shapiro, 2006;Kiekebusch et al, 2012), Corynebacterium glutamicum (Donovan et al, 2010), Myxococcus xanthus (Treuner-Lange et al, 2013;Schumacher et al, 2017), Xanthomonas citri (Lorenzoni et al, 2017) and Vibrio cholerae (Galli et al, 2016). One such example of a ParA-like protein is MinD, a part of the Min-system.…”

Section: Introductionmentioning

confidence: 99%

A cell length‐dependent transition in MinD‐dynamics promotes a switch in division‐site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells

Muraleedharan

Freitas

Mann

et al. 2018

Molecular Microbiology

View full text Add to dashboard Cite

Vibrio parahaemolyticus exists as swimmer and swarmer cells, specialized for growth in liquid and on solid environments respectively. Swarmer cells are characteristically highly elongated due to an inhibition of cell division, but still need to divide in order to proliferate and expand the colony. It is unknown how long swarmer cells divide without diminishing the population of long cells required for swarming behavior. Here we show that swarmer cells divide but the placement of the division site is cell length-dependent; short swarmers divide at mid-cell, while long swarmers switch to a specific non-mid-cell placement of the division site. Transition to non-mid-cell positioning of the Z-ring is promoted by a cell length-dependent switch in the localization-dynamics of the division regulator MinD from a pole-to-pole oscillation in short swarmers to a multi-node standing-wave oscillation in long swarmers. Regulation of FtsZ levels restricts the number of divisions to one and SlmA ensures sufficient free FtsZ to sustain Z-ring formation by preventing sequestration of FtsZ into division deficient clusters. By limiting the number of division-events to one per cell at a specific non-mid-cell position, V. parahaemolyticus promotes the preservation of long swarmer cells and permits swarmer cell division without the need for dedifferentiation.

show abstract

Section: Introductionmentioning

confidence: 99%

A cell length‐dependent transition in MinD‐dynamics promotes a switch in division‐site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells

Muraleedharan

Freitas

Mann

et al. 2018

Molecular Microbiology

View full text Add to dashboard Cite

show abstract

“…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 spindle apparatus [3]) or reaction-diffusion models [8][9][10][11][12][13][14][15]. Recent superresolution microscopy experiments have been unable to observe filamentous structures of ParA [5,13], disfavoring polymerization-based models [12].…”

mentioning

confidence: 99%

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

et al. 2017

View full text Add to dashboard Cite

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...

show abstract

“…Two of these residues (R195 and R224) are conserved in several other ParA-like ATPases (Fig. S10), and one or both of their counterparts have previously been implicated in the DNA-binding activity of other ParA homologs (28,35,37), PpfA (20), and PomZ (17). Moreover, the residues equivalent to R221, V223, R224 and K241 are in direct contact with DNA in the crystal structure of HpParA (37), indicating an excellent agreement between the HDX and crystallographic data.…”

Section: Discussionmentioning

confidence: 99%

“…The prototypical ParA homologs, for instance, mediate the partitioning of sister chromosomes and plasmids during cell division (9,12). Several other members of this family (MipZ, MinD, PldP and PomZ) ensure proper division site placement by controlling the polymerization of the cell division protein FtsZ into the cytokinetic FtsZ ring (6,8,(13)(14)(15)(16)(17).…”

Section: Introductionmentioning

confidence: 99%

“…Residues homologous to these arginines were later also implicated in the DNA-binding activity of PpfA from Rhodobacter sphaeroides and PomZ from Myxococcus xanthus (17,20). More evidence for the importance of positively charged amino acids has recently come from the crystal structures of ParA-DNA complexes formed by ParA homologs from Helicobacter pylori (HpParA) (37) and Sulfolobus solfataricus pNOB8 (38), which each identified several surface-exposed lysine residues that are in direct contact with the DNA ligand.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Molecular architecture of the DNA‐binding sites of the P‐loop ATPases MipZ and ParA fromCaulobacter crescentus

Refes

Corrales-Guerrero

et al. 2019

Preprint

View full text Add to dashboard Cite

Two related P-loop ATPases, ParA and MipZ, mediate the spatiotemporal regulation of chromosome segregation and cell division in Caulobacter crescentus. Both of these proteins share the ability to form dynamic concentration gradients that control the positioning of regulatory targets within the cell. Their proper localization relies on their nucleotide-dependent cycling between a monomeric and a dimeric state, driven by interaction with the chromosome partitioning protein ParB, and on the ability of the dimeric species to associate non-specifically with the nucleoid. In this study, we use a combination of genetic screening, biochemical analysis and hydrogen/deuterium exchange mass spectrometry to identify the residues mediating the interaction of MipZ with DNA. Our results show that the DNA-binding activity of MipZ relies on a series of positively charged and hydrophobic residues lining both sides of the dimer interface. MipZ thus appears to associate with DNA in a sequence-independent manner through electrostatic interactions with the DNA phosphate backbone. In support of this hypothesis, chromatin immunoprecipitation analyses did not reveal any specific target sites in vivo. When extending our analysis to ParA, we found that the architectures of the MipZ and ParA DNA-binding sites are markedly different, although their relative positions on the dimer surface and their mode of DNA binding are conserved. Importantly, bioinformatic analysis suggests that the same principles apply to other members of the P-loop ATPase family. ParA-like ATPases thus share common mechanistic features, although their modes of action have diverged considerably during the course of evolution. SIGNIFICANCEParA-like P-loop ATPases are involved in a variety of cellular processes in bacteria, including chromosome and plasmid segregation, chemoreceptor and carboxysome positioning, and division site placement. Many members of this large protein family depend on the ability to bind non-specific DNA for proper function.Although previous studies have yielded insights in the DNA-binding properties of some ParA-like ATPases, a comprehensive view of the underlying mechanisms is still lacking. Here, we combine state-of-the-art cell biological, biochemical and biophysical approaches to localize the DNA-binding regions of the ParA-like ATPases MipZ and ParA from Caulobacter crescentus. We show that the two proteins use the same interface and mode of action to associate with DNA, suggesting that the mechanistic basis of DNA binding may be conserved in the ParA-like ATPase family.

show abstract

The PomXYZ Proteins Self-Organize on the Bacterial Nucleoid to Stimulate Cell Division

Cited by 69 publications

References 67 publications

A cell length‐dependent transition in MinD‐dynamics promotes a switch in division‐site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells

A cell length‐dependent transition in MinD‐dynamics promotes a switch in division‐site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells

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

Molecular architecture of the DNA‐binding sites of the P‐loop ATPases MipZ and ParA fromCaulobacter crescentus

Contact Info

Product

Resources

About