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

Deepak Anand,Dominik Schumacher,Lotte Søgaard‐Andersen

doi:10.1111/mmi.14583

Deepak Anand, Dominik Schumacher + Show 1 more

Open Access

https://doi.org/10.1111/mmi.14583

Copy DOI

Abstract

In bacteria, ParABS systems and structural maintenance of chromosome (SMC) condensin-like complexes are important for chromosome segregation and organization. The rod-shaped Myxococcus xanthus cells have a unique chromosome arrangement in which a scaffold composed of the BacNOP bactofilins and PadC positions the essential ParB∙parS segregation complexes and the DNA segregation ATPase ParA in the subpolar regions. We identify the Smc and ScpAB subunits of the SMC complex in M. xanthus and demonstrate that SMC is conditionally essential, with Δsmc or ΔscpAB mutants being temperature sensitive. Inactivation of SMC caused defects in chromosome segregation and organization. Lack of the BacNOP/PadC scaffold also caused chromosome segregation defects but this scaffold is not essential for viability. Inactivation of SMC was synthetic lethal with lack of the BacNOP/PadC scaffold. Lack of SMC interfered with formation of the BacNOP/PadC scaffold while lack of this scaffold did not interfere with chromosome association by SMC. Altogether, our data support that three systems function together to enable chromosome segregation in M. xanthus. ParABS constitutes the basic and essential machinery. SMC and the BacNOP/PadC scaffold have different yet redundant roles in chromosome segregation with SMC supporting individualization of daughter chromosomes and BacNOP/PadC making the ParABS system operate more robustly.

Highlights

Chromosome segregation is closely coordinated with cell division to ensure that daughter cells inherit the correct chromosome complement
Orthologs of M. xanthus Smc, ScpA and ScpB with high sequence identity/similarity were identified in Myxoccocales with fully sequenced genomes (Fig. S3AB) and the neighborhood of the M. xanthus genes was conserved in other Myxococcales (Fig. S3AB)
To assess the function of Smc, ScpA and ScpB in M. xanthus we considered that smc mutations can cause temperature sensitive growth defects being lethal at increased temperatures

Summary

Introduction

Chromosome segregation is closely coordinated with cell division to ensure that daughter cells inherit the correct chromosome complement. Bacterial chromosomes are highly compacted and organized to fit into the confines of cells while still allowing DNA replication, repair, recombination and segregation to occur (Badrinarayanan et al, 2015, Dame et al., 2020). This organization includes positioning of individual chromosomal loci to the same subcellular locations in each cell cycle and is established during segregation (Viollier et al., 2004). Two systems have key functions in chromosome organization and segregation in bacteria, ParABS system (Badrinarayanan et al, 2015, Wang et al, 2013) and the Structural Maintenance of Chromosomes (SMC) condensin-like complex (Badrinarayanan et al, 2015, Dame et al, 2020, Nolivos & Sherratt, 2014)

Methods

Results

Conclusion