A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole

Division of Infectious Diseases, Brigham and Women's Hospital.
Genes & development (Impact Factor: 10.8). 10/2012; 26(20):2348-60. DOI: 10.1101/gad.199869.112
Source: PubMed


The cell poles constitute key subcellular domains that are often critical for motility, chemotaxis, and chromosome segregation in rod-shaped bacteria. However, in nearly all rods, the processes that underlie the formation, recognition, and perpetuation of the polar domains are largely unknown. Here, in Vibrio cholerae, we identified HubP (hub of the pole), a polar transmembrane protein conserved in all vibrios, that anchors three ParA-like ATPases to the cell poles and, through them, controls polar localization of the chromosome origin, the chemotactic machinery, and the flagellum. In the absence of HubP, oriCI is not targeted to the cell poles, chemotaxis is impaired, and a small but increased fraction of cells produces multiple, rather than single, flagella. Distinct cytoplasmic domains within HubP are required for polar targeting of the three ATPases, while a periplasmic portion of HubP is required for its localization. HubP partially relocalizes from the poles to the mid-cell prior to cell division, thereby enabling perpetuation of the polar domain in future daughter cells. Thus, a single polar hub is instrumental for establishing polar identity and organization.


Available from: Matthew K Waldor
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    • "asmussen et al . , 2007 ) . Moreover , the chromosomal position of genes determines the relative copy number during growth thereby impacting the bacteriums physiology ( Soler - Bistue et al . , 2015 ) . Notably , mechanistic aspects of chromosome organization , architecture , and cell cycle - dependent dynamics are only starting to be deciphered ( Yamaichi et al . , 2012 ; Demarre et al . , 2014 ) . The elucidation of the mechanisms that coordinate the interplay between chromosomes , accessory replicons , mobile DNA and HGT mechanisms is essential to better apprehend the evolution and niche adaptation of Vibrio species ."
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    ABSTRACT: Global change has caused a worldwide increase in reports of Vibrio-associated diseases with ecosystem-wide impacts on humans and marine animals. In Europe, higher prevalence of human infections followed regional climatic trends with outbreaks occurring during episodes of unusually warm weather. Similar patterns were also observed in Vibrio-associated diseases affecting marine organisms such as fish, bivalves and corals. Basic knowledge is still lacking on the ecology and evolutionary biology of these bacteria as well as on their virulence mechanisms. Current limitations in experimental systems to study infection and the lack of diagnostic tools still prevent a better understanding of Vibrio emergence. A major challenge is to foster cooperation between fundamental and applied research in order to investigate the consequences of pathogen emergence in natural Vibrio populations and answer federative questions that meet societal needs. Here we report the proceedings of the first European workshop dedicated to these specific goals of the Vibrio research community by connecting current knowledge to societal issues related to ocean health and food security.
    Frontiers in Microbiology 08/2015; 6. DOI:10.3389/fmicb.2015.00830 · 3.99 Impact Factor
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    • "Many studies on Par homologues (plasmid and chromosomally encoded) have demonstrated a role for a dynamic ParA scaffold and the importance of ParA–ParB interactions in bacterial DNA segregation (reviewed by Gerdes et al., 2010; Banigan et al., 2011; Hwang et al., 2013; Lim et al., 2014; Scholefield et al., 2011; Vecchiarelli et al., 2013). In the case of chromosomally encoded Par proteins, their roles in regulation of other cellular processes in a species-specific manner were also demonstrated (Kadoya et al., 2011; Murray & Errington, 2008; Scholefield et al., 2011; Thanbichler & Shapiro, 2006; Yamaichi et al., 2012). Whilst the ParB homologues have been dissected with respect to DNA binding, and dimerization/oligomerization domains, and in many cases the domains of interactions with the ParA homologues identified (Ah-Seng et al., 2009; Barillà et al., 2007; Bartosik et al., 2004; Figge et al., 2003; Kim & Shim, 1999; Leonard et al., 2004; Lukaszewicz et al., 2002; Scholefield et al., 2011; Surtees & Funnell, 1999), less is known about regions of ParA homologues involved in reciprocal interactions with the cognate partners (Jakimowicz et al., 2007; Leonard et al., 2005; Ravin et al., 2003; Scholefield et al., 2011). "
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    ABSTRACT: P. aeruginosa ParA belongs to a large subfamily of Walker-type ATPases acting as partitioning proteins in bacteria. ParA has the ability to both self-associate and interact with its partner ParB. Analysis of the deletion mutants defined the part of the protein involved in dimerization and interactions with ParB. Here, a set of the ParA alanine substitution mutants in the region between E67 and L85 was created and analyzed in vivo and in vitro. All mutants impaired in dimerization (substitutions at positions M74, H79, Y82, L84) were also defective in interactions with ParB suggesting that ParA-ParB interactions depend on the ability of ParA to dimerize. Mutants with alanine substitutions at positions E67, C68, L70, E72, F76, Q83 and L85 were not impaired in dimerization but defective in interactions with ParB. The dimerization interface partly overlaps the pseudo-hairpin, involved in interactions with ParB. ParA mutant derivatives tested in vitro showed no defects in ATPase activity. Two parA alleles, parA84, whose product can neither self-interact nor interact with ParB, and parA67, whose product is impaired in interactions with ParB but not in dimerization, were introduced into P. aeruginosa chromosome by homologous gene exchange. Both mutants showed defective separation of ParB foci but to different extents. Only PAO1161 parA84 was visibly impaired in chromosome segregation, growth rate and motilities similarly to a parAnull mutant.
    Microbiology 08/2014; 160(Pt 11). DOI:10.1099/mic.0.081216-0 · 2.56 Impact Factor
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    • "Polarly localized HubP interacts directly with the ParA1 ATPase, which is involved in segregation of chromosome 1 (Fogel and Waldor, 2006), and the ParA ATPase FlhG, which regulates flagellar assembly together with the GTPase FlhF (Fig. 3 C; Correa et al., 2005; Yamaichi et al., 2012). HubP also recruits—but does not directly interact with—the ParA ATPase ParC, which is required for the polar recruitment of chemotaxis proteins (Fig. 3 C; Ringgaard et al., 2011; Yamaichi et al., 2012). ParC, in turn, recruits the ParP protein to the pole by direct interaction , and ParP as well as ParC interact with the CheA kinase , in that way stimulating the formation of a large complex of chemotaxis proteins at the pole (Ringgaard et al., 2014). "
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    ABSTRACT: Bacteria are polarized cells with many asymmetrically localized proteins that are regulated temporally and spatially. This spatiotemporal dynamics is critical for several fundamental cellular processes including growth, division, cell cycle regulation, chromosome segregation, differentiation, and motility. Therefore, understanding how proteins find their correct location at the right time is crucial for elucidating bacterial cell function. Despite the diversity of proteins displaying spatiotemporal dynamics, general principles for the dynamic regulation of protein localization to the cell poles and the midcell are emerging. These principles include diffusion-capture, self-assembling polymer-forming landmark proteins, nonpolymer forming landmark proteins, matrix-dependent self-organizing ParA/MinD ATPases, and small Ras-like GTPases.
    The Journal of Cell Biology 07/2014; 206(1):7-17. DOI:10.1083/jcb.201403136 · 9.83 Impact Factor
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