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  • Review Article
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DNA motifs that sculpt the bacterial chromosome

Nature Reviews Microbiology volume 9, pages 15–26 (2011)Cite this article

Subjects

Key Points

  • During the bacterial cell cycle, chromosome replication, DNA segregation, DNA repair and cell division are coordinated by precisely defined events. A striking feature common to these processes is that non-coding DNA motifs with non-random chromosomal distributions play a central part. Thus, chromosome organization is reflected in the DNA sequence.

  • Motifs usually interact with a specific protein, which may or not be known. Motifs can be organized into several categories according to their function: those involved in chromosome replication and repair (DnaA boxes, and GATC, Ter and Chi (crossover hot spot instigator) motifs), those involved in chromosome organization, DNA segregation and cell division (parS, migS, KOPS (FtsK-orienting polar sequences; also known as FRS), SRS (SpoIIIE recognition sequences), matS and NBS (Noc-binding sites) motifs, and ram (RacA-binding motif) sites) and those involved in natural transformation (DUS (DNA uptake sequences) and USS (uptake signal sequences) motifs).

  • The distribution of motifs on their cognate chromosome is crucial to their activity and can be quantified using different statistical methods. Thus, it is possible to assess whether a motif is more frequent than expected (over-representation), significantly enriched on one strand versus the other (skew), more frequent in one region of the chromosome than elsewhere (domain enrichment) or clustered at specific positions (clustering). Most motifs show an exceptional distribution in at least one of these criteria, and this can also be used to predict new motifs.

  • Several examples suggest that selection acts on the overall distribution of the motifs described here rather than on individual sites. Moreover, such distribution properties, in turn, probably affect bacterial genome evolution.

Abstract

During the bacterial cell cycle, the processes of chromosome replication, DNA segregation, DNA repair and cell division are coordinated by precisely defined events. Tremendous progress has been made in recent years in identifying the mechanisms that underlie these processes. A striking feature common to these processes is that non-coding DNA motifs play a central part, thus 'sculpting' the bacterial chromosome. Here, we review the roles of these motifs in the mechanisms that ensure faithful transmission of genetic information to daughter cells. We show how their chromosomal distribution is crucial for their function and how it can be analysed quantitatively. Finally, the potential roles of these motifs in bacterial chromosome evolution are discussed.

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Figure 1: Schematic description of the bacterial cell cycle.
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Figure 2: Motifs implicated in replication and repair.
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Figure 3: Motifs implicated in chromosome segregation and cell division.
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Acknowledgements

We thank Y. Yamaichi for helpful discussion and O. Espeli for critical reading of the manuscript, and are indebted to D. Rudner for critical reading and many thoughtful discussions on the manuscript. We are grateful to the INRA MIGALE bioinformatics platform for providing computational resources. This work was supported by the French Agence Nationale de la Recherche project CoCoGen (BLAN07-1 185484).

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Authors and Affiliations

  1. INRA, UMR 1319, Institut Micalis, FR-78352, Jouy-en-Josas, France

    Fabrice Touzain, Marie-Agnès Petit & Meriem El Karoui

  2. INRA, UR1077, Mathématique, Informatique et Génome, FR-78352, Jouy-en-Josas, France

    Sophie Schbath

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  1. Fabrice Touzain
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  2. Marie-Agnès Petit
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Correspondence to Meriem El Karoui.

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Glossary

ori

The unique locus in bacterial chromosomes where DNA replication starts. Often called oriC.

Replisome

A multiprotein complex assembled at ori that contains all the enzymes necessary for replication.

Homologous recombination

A process that involves strand exchange (recombination) between DNA molecules of identical sequences. It allows faithful repair of double-strand breaks using a homologous DNA molecule as a template to repair the broken chromosome. Homology detection is mediated by RecA–Rad51 universal recombinase family members.

Terminus

A large region opposite the origin (ori) where the two replication forks fuse and bidirectional replication stops (in bacteria). This is mediated by the Ter motifs that define a 'replication fork trap' and restrict fork fusion to the terminus. In Escherichia coli, the TER macrodomain overlaps the terminus region and shows a specific segregation pattern, but it is not directly involved in replication termination.

Chromosome dimer

One large molecule containing two fully replicated chromosomes resulting from homologous recombination between duplicated chromosome arms.

dif

A unique site on the bacterial chromosome that is located in the replication termination region and is where specific recombination takes place to resolve a chromosome dimer.

Cytokinesis

Separation of the cytoplasm of the two daughter cells.

Sigma factor

A transcription initiation factor that enables the binding of RNA polymerase to gene promoters.

Nucleoid

The compact structure formed by the folded bacterial chromosome.

ChIP–chip

Chromatin immunoprecipitation followed by microarray hybridization. This technique identifies chromosome regions bound by a specific protein on a genome-wide scale.

Centromere

The region of a chromosome that is attached to the spindle during nuclear division. Bacteria have no spindle, so the term 'centromere-like' refers to a DNA region stimulating proper chromosome segregation.

Sporulation

A developmental process that leads, through asymmetrical division, to the formation of a small, dormant and very resistant cell called a spore.

Site-specific recombination

A process whereby DNA strand exchange occurs only at a specific locus. It requires specialized proteins that recognize a short specific sequence and catalyse the strand exchange reaction.

ChAP–chip

Chromatin affinity precipitation followed by microarray hybridization. This is essentially the same principle as chromatin immunoprecipitation–chip, but uses protein purification techniques that do not require protein-specific antibodies (such as tagging the protein of interest).

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Touzain, F., Petit, MA., Schbath, S. et al. DNA motifs that sculpt the bacterial chromosome. Nat Rev Microbiol 9, 15–26 (2011). https://doi.org/10.1038/nrmicro2477

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