Rules and Exceptions: The Role of Chromosomal ParB in DNA Segregation and Other Cellular Processes

Abstract

The segregation of newly replicated chromosomes in bacterial cells is a highly coordinated spatiotemporal process. In the majority of bacterial species, a tripartite ParAB-parS system, composed of an ATPase (ParA), a DNA-binding protein (ParB), and its target(s) parS sequence(s), facilitates the initial steps of chromosome partitioning. ParB nucleates around parS(s) located in the vicinity of newly replicated oriCs to form large nucleoprotein complexes, which are subsequently relocated by ParA to distal cellular compartments. In this review, we describe the role of ParB in various processes within bacterial cells, pointing out interspecies differences. We outline recent progress in understanding the ParB nucleoprotein complex formation and its role in DNA segregation, including ori positioning and anchoring, DNA condensation, and loading of the structural maintenance of chromosome (SMC) proteins. The auxiliary roles of ParBs in the control of chromosome replication initiation and cell division, as well as the regulation of gene expression, are discussed. Moreover, we catalog ParB interacting proteins. Overall, this work highlights how different bacterial species adapt the DNA partitioning ParAB-parS system to meet their specific requirements.

Activation of a signaling pathway by the physical translocation of a chromosome

“…Homologs of ChpT, PopZ, and the parS/ParB/ParA system are found throughout the α-proteobacteria and could work in similar ways. The Par system is found even more broadly and it has become increasingly clear that ParB and ParA can interact with a wide variety of proteins other than each other (Thanbichler and Shapiro, 2006;Gruber and Errington, 2009;Schofield et al, 2010;Mercy et al, 2019;Kawalek et al, 2020;Pióro and Jakimowicz, 2020), and so could participate in the regulated recruitment of proteins in other contexts and for other purposes.…”

Chromosome Segregation Proteins as Coordinators of Cell Cycle in Response to Environmental Conditions

“…The ParA and ParB proteins are components of the tripartite segregation system, which also involves parS sequences bound by ParB (parABS system) (Schumacher, 2008;Badrinarayanan et al, 2015). From 1 to 20 parS sequences, depending on the bacterial species, may be scattered over the oriC-proximal chromosomal region, which encompasses a range from 10 kb (in Caulobacter crescentus) to 200 kb in Streptomyces coelicolor, or even up to 650 kb in Pseudomonas aeruginosa (Jakimowicz et al, 2002;Livny et al, 2007;Tran et al, 2018;Kawalek et al, 2020). Upon interaction with ParB, the parS sequencerich region engages in the formation of a large nucleoprotein complex named the segrosome (Funnell, 2014;Oliva, 2016).…”

“…xanthus ParA Bactofilin-PadC (Lin et al, 2017) R. sphaeroides ParB MipZ (Dubarry et al, 2019) S. coelicolor ParA Scy (Ditkowski et al, 2013) ParJ (Ditkowski et al, 2010) ParB TopA (Szafran et al, 2013) S. pneumoniae ParB SMC (Minnen et al, 2011) CpsD (Nourikyan et al, 2015) V. cholerae ParAI HubP (Yamaichi et al, 2012) The variety of roles played by segregation proteins in the cell cycles of various bacterial species manifests in the plethora of phenotypes resulting from parAB deletion. While parAB genes were demonstrated to be essential in C. crescentus and M. xanthus, in a number of other bacterial species, including B. subtilis, P. aeruginosa, M. smegmatis, and C. glutamicum, elimination of ParA or ParB leads to chromosome segregation aberrations and mispositioning of the oriC region, eventually resulting in the formation of from 1 to 30% anucleate cells (recently comprehensively reviewed by Kawalek et al, 2020). In some bacteria (V. cholerae and B. subtilis), parB (but not parA) deletion increases the genomic content being manifested as elevated number of oriCs (Lee et al, 2003;Kadoya et al, 2011).…”

Distinct activities of bacterial condensins for chromosome management in Pseudomonas aeruginosa

“…ParB is a CTP hydrolase whose activity is critical for its interaction with parS (Jalal et al, 2020;Osorio-Valeriano et al, 2019;Soh et al, 2019). The resulting ParB/parS nucleoprotein complex encompasses several kbs of DNA and interacts with the ParA ATPase that drives its segregation (Kawalek et al, 2020). The ParB-parS complex also recruits Smc-ScpAB onto the chromosome (Gruber and Errington, 2009;Sullivan et al, 2009).…”