SMC complexes organize the bacterial chromosome by lengthwise compaction
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MINI-REVIEW
SMC complexes organize the bacterial chromosome by lengthwise compaction Jarno Mäkelä1 · David Sherratt1 Received: 27 March 2020 / Revised: 2 April 2020 / Accepted: 4 April 2020 © The Author(s) 2020
Abstract Structural maintenance of chromosomes (SMC) complexes are ancient and conserved molecular machines that organize chromosomes in all domains of life. We propose that the principles of chromosome folding needed to accommodate DNA inside a cell in an accessible form will follow similar principles in prokaryotes and eukaryotes. However, the exact contributions of SMC complexes to bacterial chromosome organization have been elusive. Recently, it was shown that the SMC homolog, MukBEF, organizes and individualizes the Escherichia coli chromosome by forming a filamentous axial core from which DNA loops emanate, similar to the action of condensin in mitotic chromosome formation. MukBEF action, along with its interaction with the partner protein, MatP, also facilitates chromosome individualization by directing opposite chromosome arms (replichores) to different cell halves. This contrasts with the situation in many other bacteria, where SMC complexes organise chromosomes in a way that the opposite replichores are aligned along the long axis of the cell. We highlight the similarities and differences of SMC complex contributions to chromosome organization in bacteria and eukaryotes, and summarize the current mechanistic understanding of the processes. Keywords Chromosome organization · Escherichia coli · SMC complex · MukBEF
Overview In all domains of life, incredibly long genomic DNAs must be folded into higher order looped structures to accommodate DNA inside a cell. The processes that manage DNA, whether it be replication, repair, gene expression, or chromosome segregation, must act on DNA in a way that the processes sense whether they are acting on the same or different molecules by tracking the three-dimensional path of individual DNA molecules. A single class of conserved and ancient proteins, structural maintenance of chromosomes (SMC) complexes, play multiple important roles in chromosome organization and individualization [reviewed in (Yatskevich et al. 2019)]. Although Escherichia coli MukB was Communicated by M. Kupiec. * David Sherratt [email protected] Jarno Mäkelä [email protected] 1
the first SMC protein to be identified through its role in chromosome segregation (Hiraga et al. 1989), much subsequent work has focussed on eukaryote condensins and cohesins, initially implicated in mitotic chromosome compaction and sister chromosome cohesion, respectively. The distinctive architectures and classes of SMC complexes are shown schematically in Fig. 1. Given the conservation of SMC complexes, it is unescapable to propose that they share common mechanisms of action, although these mechanisms have remained elusive and controversial. Nevertheless, recent demonstrations that both purified condensin and cohesin can extrude DNA loops, dependent on ATP hydrolysis, in single-mo
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