Bacterial chromatin

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Recent studies have revealed that the bacterial nucleoid is a dynamic entity that alters its overall structure in response to changes in both growth rate and growth phase. These structural changes are correlated with, and might be driven by, changes in the distribution and utilization of DNA supercoiling. In turn, these parameters in addition to the delimitation of topological domains are dependent both on the relative proportions of the abundant nucleoid-associated proteins and on transcriptional activity. The domain structure itself is dynamic.

Introduction

The bacterial nucleoid is a dynamic structure, the organization of which must adapt both to varying rates of replication and also to the different transcriptional requirements that are a consequence of changes in external environmental conditions. A single Escherichia coli chromosome comprises 4.6 Mb and must be compacted at least ∼1000-fold to fit inside the bacterial cell. The requirements of compaction and varying gene expression imply that bacterial chromatin, whether containing a replicating or a non-replicating chromosome, must, like eukaryotic chromatin, possess a high degree of spatial organization.

What is the nature of chromosomal organization and how is it imposed? In the past two years it has become apparent that the maintenance and use of negative supercoils in the DNA is central to both issues. Negative supercoiling can facilitate both DNA folding and compaction — as in the archetypal example of the eukaryotic nucleosome — and also the untwisting of DNA, which is required for the initiation of transcription and replication, in addition to DNA recombination. In the bacterial cell, the abundant nucleoid-associated proteins, including FIS (factor for inversion stimulation), H-NS (heat-stable [or histone-like] nucleoid-structuring), HU (heat-unstable), Dps (DNA-binding protein from starved cells) and IHF (integration host factor) (Table 1) function to package DNA and to dynamically constrain superhelicity.

In this review, we discuss recent developments linking the properties of superhelical domains to the spatial organisation of the bacterial chromosome.

Section snippets

Topological domains

There is abundant evidence that chromosomal DNA is organized into topological domains, which are insulated from their immediate neighbours. The extent of these domains has, until recently, been ill-defined but was initially believed to be approximately 50 to 100 kb [1]. One approach to a more precise determination of domain size is to alter local, rather than global, topology. Postow et al. [2••] accomplished this by the elegant technique of expressing the restriction enzyme SwaI in vivo to

Chromosome dynamics and the nature of topological barriers

The dynamic nature of topological domains implies that the barriers separating them must also be transient. Barriers are defined functionally as entities that prevent the free diffusion of supercoils. In principle a barrier could be created by tethering the DNA duplex either to RNA or to a protein, and thereby preventing free rotation. Another, not exclusive, possibility is that supercoils generated by transcription or a translocating enzyme could be dissipated by the binding of a topoisomerase

Macrodomain (and higher) organization

The correlation between the size of putative topological domains and the transcriptional activities has been emphasized by a recent study by Jeong et al. [10], who analysed the transcriptional properties of the E. coli genome as a function of the position of genes on the chromosome. These authors observed that the short-range pattern of transcriptional activity sensitive to gyrase function extended up to 16 kb. However, in addition, they detected two other patterns of transcriptional activity, a

Negative superhelicity and gene expression

Three independent lines of evidence now point to the important conclusion that negative supercoiling is a crucial determinant of the pattern of gene expression in the bacterial cell and that the available superhelicity is controlled by a homeostatic interconnected regulatory network that includes not only topoisomerases and the abundant nucleoid-associated proteins but also RNA polymerase and effectors that directly modify the properties of the enzyme. The implication is that, as in eukaryotes,

The role of nucleoid-associated proteins

Crucial to the organization of bacterial chromatin are the relative amounts of the different, abundant nucleoid-associated proteins. Not only do these amounts vary with growth phase [34] but also the expression of any one of these proteins is regulated by one or more of the others. In early exponential phase, FIS, HUα2 and H-NS predominate, to be succeeded by HUαβ and H-NS in the transition between exponential and stationary phase, and finally by IHF and Dps in late stationary phase. These

Conclusions and future directions

Despite the very different composition of bacterial and eukaryotic chromatin, there are some intriguing parallels. The delimitation of topological domains by DNA gyrase and topoisomerase IV in bacteria is reminiscent of the association of topoisomerase II with the eukaryotic nuclear matrix. Similarly, the occurrence of dynamic transcription factories in close spatial proximity appears to occur in both types of chromatin.

In bacteria, recent studies have emphasized the central role of DNA

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Glossary

Counterions
Positively charged ions that neutralize the negative charges of DNA phosphates.
Pathogenicity islands
Spatially separated regions of the genome that are enriched in genes associated with bacterial pathogenicity. These islands have a distinctive GC content and are usually flanked by mobile DNA elements.
Plectonemic loops
The loops generated by the intertwining of two DNA duplexes within a single supercoiled DNA molecule.
Replichore
The segment of the bacterial chromosome from origin to

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