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The bacterial segrosome: a dynamic nucleoprotein machine for DNA trafficking and segregation

Nature Reviews Microbiology volume 4, pages 133–143 (2006)Cite this article

Key Points

  • Genome segregation is a fundamental process that all cells must perform with high accuracy and in precise coordination with other cell-cycle events. The molecular mechanisms that underpin plasmid and chromosome segregation in prokaryotes are the subject of intense investigation.

  • The segrosome is the nucleoprotein molecular machine that directs the intracellular movement of plasmids during segregation. Plasmid segregation requires a pair of proteins that interacts with a centromere analogue. One protein is most commonly a member of the ParA superfamily of Walker-type ATPases, whereas the partner protein is a DNA-binding factor that interacts site-specifically with the plasmid centromere analogue.

  • Plasmid centromeres have diverse organizations, although all centromeres contain repeat motifs that are recognized by the DNA-binding protein. The ParA protein does not contact the centromere directly, but is instead recruited into the segrosome complex by the DNA-binding factor.

  • Although their mode of action remains to be fully elucidated, there is growing evidence that ParA proteins can polymerize into extensive filamentous structures. Polymerization is controlled by nucleotide binding and hydrolysis, as well as by the partner protein. ParA polymerization within the segrosome could move plasmids in bipolar orientations during segregation.

  • The tertiary structures of several partition proteins have recently been solved, providing invaluable new insights into segrosome organization and assembly.

Abstract

The genomes of unicellular and multicellular organisms must be partitioned equitably in coordination with cytokinesis to ensure faithful transmission of duplicated genetic material to daughter cells. Bacteria use sophisticated molecular mechanisms to guarantee accurate segregation of both plasmids and chromosomes at cell division. Plasmid segregation is most commonly mediated by a Walker-type ATPase and one of many DNA-binding proteins that assemble on a cis-acting centromere to form a nucleoprotein complex (the segrosome) that mediates intracellular plasmid transport. Bacterial chromosome segregation involves a multipartite strategy in which several discrete protein complexes potentially participate. Shedding light on the basis of genome segregation in bacteria could indicate new strategies aimed at combating pathogenic and antibiotic-resistant bacteria.

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Figure 1: Genetic organization of plasmid segregation gene cassettes.
Figure 2: The diverse organization of plasmid centromeres.
Figure 3: Tertiary structures of segregation proteins.
Figure 4: Comparative sequence organization of selected ParA superfamily proteins.
Figure 5: Speculative model for segregation of plasmids that encode ParA proteins.

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Acknowledgements

Work in the authors' laboratories is supported by The Wellcome Trust and Biotechnology & Biological Sciences Research Council (F.H.), and the Medical Research Council and Royal Society (D.B.). We thank S. Austin and D. Summers for helpful comments on an early draft of the manuscript.

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Authors and Affiliations

  1. Faculty of Life Sciences, University of Manchester, Jackson's Mill, PO BOX 88, Sackville Street, Manchester, M60 1QD, UK

    Finbarr Hayes

  2. Department of Biology, University of York, PO BOX 373, York, YO10 5YW, UK

    Daniela Barillà

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Correspondence to Finbarr Hayes or Daniela Barillà.

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DATABASES

Entrez Genome Project

Bacillus subtilis

Escherichia coli

Thermus thermophilus

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Daniela Barillà's homepage:

Glossary

Actin, tubulin and intermediate filaments

Cytoskeletal proteins that are involved in a range of biological processes in eukaryotic cells. Ancestral homologues of these proteins are now known to exist in bacteria in which they are implicated in plasmid and chromosome partition, among other functions.

Segrosome

A nucleoprotein complex that mediates genome segregation in bacteria.

Site-specific recombinases

DNA-cleavage and rejoining enzymes required for various DNA transactions, including the resolution of plasmid and chromosome dimers to monomers in bacteria.

Plasmid multimers

More than one copy of a plasmid that are joined together to form a single DNA molecule. This reduces plasmid copy number and can lead to plasmid loss unless reversed by the action of site-specific recombinases.

Toxin–antitoxin

A postsegregational cell-killing system usually composed of a pair of plasmid-encoded proteins that form a complex. If a plasmid-free cell arises, the antitoxin cannot be replenished and the liberated toxin causes cell death or severe growth impairment.

Walker box ATPase motifs

Conserved amino-acid motifs that are found in the Walker-type superfamily of ATPases, and which are implicated in the binding and hydrolysis of ATP.

Incompatibility

The phenomenon whereby plasmids that replicate or segregate using identical or closely related mechanisms cannot coexist in the same cell, resulting in subpopulations that possess only one of the plasmids, but not both.

Insertional polymerization

The growth of actin polymers by the insertion of actin subunits at the leading edge of the elongating filament. Actin polymerization involves growth of the polymers at one end and concomitant disassembly at the opposite end (treadmilling).

Src homology 3 domain

(SH3). A feature of many eukaryotic signalling proteins that show specificity for proline-rich sequences. These domains have many functions, including the promotion of protein–protein interactions.

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Hayes, F., Barillà, D. The bacterial segrosome: a dynamic nucleoprotein machine for DNA trafficking and segregation. Nat Rev Microbiol 4, 133–143 (2006). https://doi.org/10.1038/nrmicro1342

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