A dynamic, mitotic-like mechanism for bacterial chromosome segregation

Abstract

The mechanisms that mediate chromosome segregation in bacteria are poorly understood. Despite evidence of dynamic movement of chromosome regions, to date, mitotic-like mechanisms that act on the bacterial chromosome have not been demonstrated. Here we provide evidence that the Vibrio cholerae ParAI and ParBI proteins are components of an apparatus that pulls the origin region of the large V. cholerae chromosome to the cell pole and anchors it there. ParBI interacts with a conserved origin-proximal, centromere-like site (parSI) that, following chromosome replication, segregates asymmetrically from one pole to the other. While segregating, parSI stretches far away from neighboring chromosomal loci. ParAI forms a dynamic band that extends from the pole to the segregating ParBI/parSI complex. Movement of ParBI/parSI across the cell occurs in concert with ParAI retraction. Deletion of parAI disrupts proper origin localization and segregation dynamics, and parSI no longer separates from nearby regions. These data suggest that ParAI forms a dynamic structure that pulls the ParBI-bound chromosome to the pole in a process analogous to anaphase of eukaryotic mitosis.[Keywords: Vibrio cholerae; chromosome segregation; ParA; ParB] Supplemental material is available at http://www.genesdev.org.

Independent Segregation of the Two Arms of theEscherichia coli oriRegion Requires neither RNA Synthesis nor MreB Dynamics

“…ParA is an ATPase that binds ParB and is proposed to direct the ParB/parS complex to the poles (18). These partitioning systems serve to facilitate chromosome segregation but are often not essential, for example, in B. subtilis, Streptomyces coelicolor, and Pseudomonas putida and for V. cholerae chromosome I (18,23,30,35).In contrast, these systems are essential for viability in C. crescentus (41,54) and for segregation of chromosome II in V. cholerae (63). The latter requirement may be due to the fact that chromosome II has many properties of a large plasmid and its Par proteins are more closely related to plasmid-encoded ones than to those encoded on chromosomes (22).…”

“…ParB is a DNA-binding protein that specifically recognizes parS and subsequently spreads along the DNA to form a nucleoprotein complex (7,37,42). ParA is an ATPase that binds ParB and is proposed to direct the ParB/parS complex to the poles (18). These partitioning systems serve to facilitate chromosome segregation but are often not essential, for example, in B. subtilis, Streptomyces coelicolor, and Pseudomonas putida and for V. cholerae chromosome I (18,23,30,35).…”

Characterization of the mycobacterial chromosome segregation protein ParB and identification of its target in Mycobacterium smegmatis

“…to the 1/4 and 3/4 positions (Escherichia coli, Bacillus subtilis, Vibro cholerae chromosome II), or one copy of the newly synthesized origins remains at the pole while the other copy migrates to the opposite pole Abbreviations: EMSA, electrophoretic mobility shift assay; GST, glutathione S-transferase; Ms, M. smegmatis; Mt, M. tuberculosis. (Caulobacter crescentus, Vibrio cholerae chromosome I) (Fogel & Waldor, 2006;Lewis, 2004;Teleman et al, 1998;Viollier et al, 2004;Webb et al, 1997).…”

“…to the 1/4 and 3/4 positions (Escherichia coli, Bacillus subtilis, Vibro cholerae chromosome II), or one copy of the newly synthesized origins remains at the pole while the other copy migrates to the opposite pole Abbreviations: EMSA, electrophoretic mobility shift assay; GST, glutathione S-transferase; Ms, M. smegmatis; Mt, M. tuberculosis. (Caulobacter crescentus, Vibrio cholerae chromosome I) (Fogel & Waldor, 2006;Lewis, 2004;Teleman et al, 1998;Viollier et al, 2004;Webb et al, 1997).Among the large number of proteins involved in chromosome segregation, ParAB homologues were the earliest to be identified and are the best studied, particularly in B. subtilis (Lewis & Errington, 1997;Lin et al, 1997;Webb et al, 1997) Besides pathogenic, slow-growing species (M. tuberculosis and Mycobacterium leprae), the genus Mycobacterium also includes saprophytic, 'fast-growing' species such as Mycobacterium smegmatis, which would be useful for studying some aspects of mycobacterial biology, including chromosome segregation. Detailed studies of mycobacterial chromosome segregation and characterization of the key molecules involved in this process may also be helpful in identifying novel drug targets.…”

From spores to antibiotics via the cell cycle

“…Similar properties were then described for plasmid ParA proteins and their respective plasmids (Møller-Jensen et al, 2000). Recent work with chromosomal ParA homologues in Vibrio or Caulobacter has provided visual evidence for an active role in origin movement (Fogel & Waldor, 2006). The molecular basis for the dynamic behaviour of Soj has now been worked out in outline (Hester & Lutkenhaus, 2007;Leonard et al, 2005;Murray & Errington, 2008) (Fig.…”