Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum

Abstract

Higher-order chromosome folding and segregation are tightly regulated in all domains of life. In bacteria, details on nucleoid organization regulatory mechanisms and function remain poorly characterized, especially in non-model species. Here, we investigate the role of DNApartitioning protein ParB and SMC condensin complexes in the actinobacterium Corynebacterium glutamicum. Chromosome conformation capture reveals SMC-mediated longrange interactions around ten centromere-like parS sites clustered at the replication origin (oriC). At least one oriC-proximal parS site is necessary for reliable chromosome segregation. We use chromatin immunoprecipitation and photoactivated single-molecule localization microscopy to show the formation of distinct, parS-dependent ParB-nucleoprotein subclusters. We further show that SMC/ScpAB complexes, loaded via ParB at parS sites, mediate chromosomal inter-arm contacts (as previously shown in Bacillus subtilis). However, the MukBEF-like SMC complex MksBEFG does not contribute to chromosomal DNA-folding; instead, this complex is involved in plasmid maintenance and interacts with the polar oriCtethering factor DivIVA. Our results complement current models of ParB-SMC/ScpAB crosstalk and show that some condensin complexes evolved functions that are apparently uncoupled from chromosome folding.

Dynamics of the compartmentalizedStreptomyceschromosome during metabolic differentiation

“…The most likely candidate to be involved in this reorganization is the Smc-ScpAB condensin complex, which is recruited to the origin region by ParB bound to parS 45,46 . From the parS sites, Smc-ScpAB promotes inter-arm contacts by translocating to the terminal region of the chromosome, likely by loop extrusion 20,21,24,27,[47][48][49][50][51][52] . Streptomyces spp.…”

“…Notably pioneer studies revealed that bacterial chromosomes present a high degree of 3D-organization in macrodomains and/or 'chromosome interacting domains' (CIDs), mediated by multiple structural factors, including transcription and replication [20][21][22][23][24][25][26][27] . Here, we explore the dynamics of the…”

SMC and the bactofilin/PadC scaffold have distinct yet redundant functions in chromosome segregation and organization in Myxococcus xanthus

“…How this effect is brought about is not known but could be a consequence of the increased length of the nucleoid‐free subpolar regions in the absence of SMC or, alternatively, a direct interaction between BacNOP/PadC and SMC. In several bacteria, the ParB∙ parS complex serves as a loading platform for SMC (Sullivan et al ., 2009; Gruber and Errington, 2009; Minnen et al ., 2011; Tran et al ., 2017; Böhm et al ., 2020; Chan et al ., 2020). Smc‐mCherry was stable in the absence of ScpAB.…”

“…The ScpA kleisin homolog reinforces ring formation while the ScpB dimer interacts with ScpA (Nolivos and Sherratt, 2014; Yatskevich et al ., 2019) (Figure 1a). Based on work in several bacteria, SMC complexes of the Smc/ScpA/ScpB type are loaded onto the two daughter chromosomes during chromosome segregation at the ParB∙ parS complexes close to ori (Sullivan et al ., 2009; Gruber and Errington, 2009; Minnen et al ., 2011; Tran et al ., 2017; Böhm et al ., 2020; Chan et al ., 2020). Each SMC complex is thought to encircle the two replichores of a daughter chromosome and translocate many kbp away from the loading site while aligning the two replichores and, in parallel, individualizing the two daughter chromosomes (Le et al ., 2013; Wang et al ., 2015; Marbouty et al ., 2015; Minnen et al ., 2016; Tran et al ., 2017; Wang et al ., 2017; Böhm et al ., 2020).…”

“…Based on work in several bacteria, SMC complexes of the Smc/ScpA/ScpB type are loaded onto the two daughter chromosomes during chromosome segregation at the ParB∙ parS complexes close to ori (Sullivan et al ., 2009; Gruber and Errington, 2009; Minnen et al ., 2011; Tran et al ., 2017; Böhm et al ., 2020; Chan et al ., 2020). Each SMC complex is thought to encircle the two replichores of a daughter chromosome and translocate many kbp away from the loading site while aligning the two replichores and, in parallel, individualizing the two daughter chromosomes (Le et al ., 2013; Wang et al ., 2015; Marbouty et al ., 2015; Minnen et al ., 2016; Tran et al ., 2017; Wang et al ., 2017; Böhm et al ., 2020). Inactivation of SMC causes defects in chromosome segregation (Niki et al ., 1991; Yamanaka et al ., 1996; Britton et al ., 1998; Moriya et al ., 1998; Jensen and Shapiro, 1999; Mascarenhas et al ., 2002; Danilova et al ., 2007; Yu et al ., 2010; Schwartz and Shapiro, 2011; Minnen et al ., 2011; Petrushenko et al ., 2011; Gruber et al ., 2014; Wang et al ., 2014; Chan et al ., 2020).…”