Article

A Self-Associating Protein Critical for Chromosome Attachment, Division, and Polar Organization in Caulobacter

Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520, USA.
Cell (Impact Factor: 33.12). 10/2008; 134(6):956-68. DOI: 10.1016/j.cell.2008.07.016
Source: PubMed

ABSTRACT Cell polarization is an integral part of many unrelated bacterial processes. How intrinsic cell polarization is achieved is poorly understood. Here, we provide evidence that Caulobacter crescentus uses a multimeric pole-organizing factor (PopZ) that serves as a hub to concurrently achieve several polarizing functions. During chromosome segregation, polar PopZ captures the ParB*ori complex and thereby anchors sister chromosomes at opposite poles. This step is essential for stabilizing bipolar gradients of a cell division inhibitor and setting up division near midcell. PopZ also affects polar stalk morphogenesis and mediates the polar localization of the morphogenetic and cell cycle signaling proteins CckA and DivJ. Polar accumulation of PopZ, which is central to its polarizing activity, can be achieved independently of division and does not appear to be dictated by the pole curvature. Instead, evidence suggests that localization of PopZ largely relies on PopZ multimerization in chromosome-free regions, consistent with a self-organizing mechanism.

Download full-text

Full-text

Available from: Ariane Briegel, Jul 29, 2015
0 Followers
 · 
121 Views
  • Source
    • "2B and C, 3A and B). This polar REZ is reminiscent of structures seen previously for an overexpression mutant of PopZ, a protein thought to anchor chromosomal origins to the pole, in Caulobacter crescentus (Ebersbach et al. 2008). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Campylobacter jejuni is one of the most successful food-borne human pathogens. Here we use electron cryotomography to explore the ultrastructure of C. jejuni cells in logarithmically growing cultures. This provides the first look at this pathogen in a near-native state at macromolecular resolution (~5 nm). We find a surprisingly complex polar architecture that includes ribosome exclusion zones, polyphosphate storage granules, extensive collar-shaped chemoreceptor arrays, and elaborate flagellar motors.
    MicrobiologyOpen 10/2014; 3(5). DOI:10.1002/mbo3.200 · 2.21 Impact Factor
  • Source
    • "s are separated presumably by ' bulk ' segregation mechanisms ( such as DNA replication , transcription , entropic unmixing , etc ) . This is followed by a fast , ParA - dependent phase , and completed by the anchoring of the partition complex at the new pole through a physical interaction between ParB and the PopZ matrix ( Bowman et al . , 2008 ; Ebersbach et al . , 2008 ; Shebelut et al . , 2010 ) ."
    [Show abstract] [Hide abstract]
    ABSTRACT: eLife digest DNA molecules exist in cells as tightly packed structures called chromosomes. During the cell cycle, chromosomes duplicate, and the two copies separate, ready to end up in two separate daughter cells. The process of chromosome separation in cells of higher organisms such as animals and plants is well understood. A protein-based structure called the spindle apparatus guides the separating chromosomes to different ends of the dividing cell. However, how chromosome separation occurs in bacteria is not well understood despite its importance in bacterial multiplication. The nucleoprotein complex ParABS is critical for separating chromosomes in bacteria. The complex is made up of three parts: parS, a stretch of DNA located at the point where chromosome duplication begins; and two proteins called ParB and ParA. While the molecular players are known, how they work together to separate chromosomes is under debate. One popular suggestion is that ParA forms a spindle-like structure. Alternatively, a diffusion-based mechanism has been proposed, where a gradient of ParA molecules bound to the chromosome interacts with a parS/ParB complex, directing the diffusion of the complex. Lim et al. used quantitative microscopy to observe the movement of the parS/ParB complex and the spatial distribution of the ParA proteins in a model bacterium. The results were inconsistent with the presence of a spindle-like structure in the cells. A mathematical model describing chromosome movement—based on the number and activity of ParA and ParB found in live cells—also failed to fit with either the spindle or the diffusion theory. Instead, Lim et al. propose a new model, based on the discovery that chromosomes are elastic. In this ‘DNA-relay model’, ParA is bound to DNA. When ParB intermittently binds to ParA, it usually catches the ParA-DNA complex when the complex is elastically stretched. The elasticity of the chromosome itself then makes the parS/ParB complex move in the direction where the most ParA molecules are still bound to the chromosome. Lim et al. suggest that similar elastic mechanisms could also be behind more general intracellular transport in bacteria. DOI: http://dx.doi.org/10.7554/eLife.02758.002
    eLife Sciences 05/2014; 3:e02758. DOI:10.7554/eLife.02758 · 8.52 Impact Factor
  • Source
    • "However, unlike DivIVA, these clusters do not appear to have an intrinsic affinity for curved membranes. Instead, they localize preferentially to subcellular regions devoid of chromosomal DNA, suggesting a role of the nucleoid in PopZ positioning [Ebersbach et al., 2008; Saberi and Emberly, 2010]. Recent work demonstrated that the characteristic cell cycle-dependent localizaton dynamics of PopZ are achieved by coupling the formation of new clusters to the segregation of the chromosomal origin regions [Laloux and Jacobs-Wagner, 2013]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Bacteria possess a diverse set of cytoskeletal proteins that mediate key cellular processes such as morphogenesis, cell division, DNA segregation and motility. Similar to eukaryotic actin or tubulin, many of them require nucleotide binding and hydrolysis for proper polymerization and function. However, there is also a growing number of bacterial cytoskeletal elements that assemble in a nucleotide-independent manner, including intermediate filament-like structures as well several classes of bacteria-specific polymers. The members of this group form stable scaffolds that have architectural roles or act as localization factors recruiting other proteins to distinct positions within the cell. Here, we highlight the elements that constitute the nucleotide-independent cytoskeleton of bacteria and discuss their biological functions in different species. © 2013 Wiley Periodicals, Inc.
    Cytoskeleton 08/2013; 70(8). DOI:10.1002/cm.21126 · 3.01 Impact Factor
Show more