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Organization and segregation of bacterial chromosomes

Nature Reviews Genetics volume 14, pages 191–203 (2013)Cite this article

Subjects

Key Points

  • The bacterial chromosome must be linearly compacted more than 1,000-fold to fit within the bacterial cell.

  • The chromosome is compacted in an orderly and hierarchical fashion in lockstep with DNA replication. This condensation has a central role in organizing replicated sister chromosomes and driving their segregation.

  • The organization of the chromosome within the bacterial cell recapitulates the genetic map.

  • Segregation of bacterial chromosomes can be broken down into three discrete steps: separation of the newly replicated origins; bulk chromosome segregation; and resolution and transport of the replication termini at the division septum.

  • In many bacteria, origin segregation is facilitated by a highly conserved partitioning system.

  • Bulk chromosome segregation is principally driven by the orderly compaction of the replicated sisters along adjacent DNA segments. This lengthwise condensation is mediated by the concerted action of supercoiling, small nucleoid-associated proteins and structural maintenance of chromosome (SMC) condensin complexes.

  • Segregation of replicated termini requires topoisomerase IV to remove catenanes and XerCD recombinase to convert chromosome dimers into monomers. Decatenation and dimer resolution are coordinated and facilitated by a septum-associated DNA translocase.

Abstract

The bacterial chromosome must be compacted more than 1,000-fold to fit into the compartment in which it resides. How it is condensed, organized and ultimately segregated has been a puzzle for over half a century. Recent advances in live-cell imaging and genome-scale analyses have led to new insights into these problems. We argue that the key feature of compaction is the orderly folding of DNA along adjacent segments and that this organization provides easy and efficient access for protein–DNA transactions and has a central role in driving segregation. Similar principles and common proteins are used in eukaryotes to condense and to resolve sister chromatids at metaphase.

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Figure 1: The bacterial nucleoid.
Figure 2: Topological organization of the bacterial chromosome.
Figure 3: Spatial organization of bacterial chromosomes.
Figure 4: Chromosome segregation viewed in three steps.

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Acknowledgements

We thank members of the Rudner laboratory for advice and encouragement, J. Marko and S. Jun for invaluable discussions, N. Kleckner for sharing unpublished data, B. Ward for expert editing and the anonymous referees for insightful critiques. Support for this work comes from the US National Institutes of Health Grant GM086466. X.W. is a long-term fellow of the Human Frontier Science Program. P.M.L. is a Helen Hay Whitney fellow.

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  1. Xindan Wang and Paula Montero Llopis: These authors contributed equally to this work.

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  1. Department of Microbiology and Immunobiology, Harvard Medical School, HIM 1025, 77 Avenue Louis Pasteur, Boston, 02115, Massachusetts, USA

    Xindan Wang, Paula Montero Llopis & David Z. Rudner

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Glossary

DNA transactions

Processes in the cell that act on DNA: for example, transcription, replication, recombination and repair.

Plectonemic loops

Also known as interwound loops, these are loops of DNA that are twisted together as a result of under- or over-winding the DNA duplex.

Decatenation

The act of unlinking interlocked (or catenated) rings.

Topoisomerases

Enzymes that modify DNA topology. Some of these enzymes affect supercoiling by under- or over-winding the DNA, whereas others decatenate interlocked rings.

DNA gyrase

A topoisomerase that introduces negative supercoils into DNA. Often referred to as gyrase. This enzyme functions by cutting both strands of the DNA, passing a looped strand of DNA through the cut site followed by resealing.

Pre-catenanes

Interlocked rings that are generated during replication. Many of these rings are unlinked before the completion of replication. Those that remain after replication is complete are called catenanes.

Sporulation

The process by which a bacterial cell differentiates into a dormant and stress-resistant cell type called a spore.

Chromosome arms

The origin and terminus of replication divide the genome into separate replicated halves. Each half is referred to as a replichore or a chromosome arm.

Septum

The structure generated during the division process that compartmentalizes a cell into two daughter cells.

Plasmid maintenance

The processes that ensure faithful inheritance of a plasmid in daughter cells.

Anucleate cells

For bacteria, refers to cells lacking a chromosome.

Catenanes

Interlocked rings (of circular chromosomes or plasmids) that cannot be separated without breaking the covalent bonds in DNA.

Dimeric chromosomes

Sister chromosomes conjoined into a single circle. Dimeric chromosomes result from an uneven number of homologous recombination events between sisters during replication.

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Wang, X., Llopis, P. & Rudner, D. Organization and segregation of bacterial chromosomes. Nat Rev Genet 14, 191–203 (2013). https://doi.org/10.1038/nrg3375

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