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Bacterial nucleoid-associated proteins, nucleoid structure and gene expression

Nature Reviews Microbiology volume 8, pages 185–195 (2010)Cite this article

Subjects

Key Points

  • The bacterial nucleoid is dynamic in nature and undergoes changes in its local and global structure as a result of DNA replication, DNA recombination and gene expression.

  • Nucleoid-associated proteins (NAPs) contribute to both the organization of the nucleoid and the control of gene expression, and it is becoming evident that NAPs and transcription act in concert to confer structure on the bacterial genome.

  • NAPs vary in the manner in which they interact with DNA, and their different binding modes facilitate positive or negative influences on transcription and also have different effects on the shape of the genetic material in the nucleoid. The bending, wrapping and bridging of DNA by NAPs contribute to the development of simple regulatory switches that control gene expression and recombination.

  • Some transcription factors such as cyclic AMP–cAMP regulatory protein (Crp), which have been classified previously as conventional transcription factors that make highly specific contacts with RNA polymerase to control transcription initiation, have been found to bind far more widely in the genome than was previously believed. This suggests that the boundary between NAPs and at least some transcription factors may be blurred and that bacteria possess a population of different DNA-binding proteins with a spectrum of DNA-binding activities.

  • Recent insights into the biology of NAPs, their roles in gene regulation and their relationships with horizontally acquired DNA are deepening our understanding of the contributions that NAPs have made, and are still making, to the evolution of the nucleoid and to the operations of the gene expression programmes therein.

Abstract

Emerging models of the bacterial nucleoid show that nucleoid-associated proteins (NAPs) and transcription contribute in combination to the dynamic nature of nucleoid structure. NAPs and other DNA-binding proteins that display gene-silencing and anti-silencing activities are emerging as key antagonistic regulators of nucleoid structure. Furthermore, it is becoming clear that the boundary between NAPs and conventional transcriptional regulators is quite blurred and that NAPs facilitate the evolution of novel gene regulatory circuits. Here, NAP biology is considered from the standpoints of both gene regulation and nucleoid structure.

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Figure 1: Nucleoid-associated proteins and DNA supercoiling influence nucleoid structure.
Figure 2: Antagonistic DNA-binding modes of nucleoid-associated proteins.
Figure 3: Nucleoid-associated protein secondary structure and domain organization.
Figure 4: Complex regulation of transcription by multiple nucleoid-associated proteins.

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Acknowledgements

We thank N. Ní Bhriain for critical comments on the manuscript. Work in the authors' laboratory is supported by grants from Science Foundation Ireland and the Wellcome Trust.

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  1. Department of Microbiology, School of Genetics and Microbiology, Moyne Institute of Preventive Medicine, Trinity College, Dublin 2, Ireland

    Shane C. Dillon & Charles J. Dorman

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Correspondence to Charles J. Dorman.

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DATABASES

Entrez Genome Project

Bacillus subtilis

Borrelia burgdorferi

Escherichia coli

Geobacillus stearothermophilus

Haemophilus influenzae

Mycobacterium tuberculosis

Pseudomonas aeruginosa

Salmonella enterica

Vibrio cholerae

FURTHER INFORMATION

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Pfam

Glossary

Stable RNA genes

Genes that code for ribosomal RNA (rRNA) and tRNA. Compared with mRNA, rRNA and tRNA are chemically very stable.

Superhelical density

The average number of superhelical turns per helical turn of the DNA, usually abbreviated as σ.

Transcription factories

Foci in the nucleoid where highly transcribed promoters, such as those of the ribosomal RNA genes, coalesce during periods of high transcriptional activity.

DNA bridging

Pertaining to a protein that binds to two distinct DNA molecules or different portions of the same DNA molecule simultaneously through two DNA-binding domains, producing a DNA–protein–DNA bridge.

Plectonemically supercoiled DNA

DNA with a braided or interwound appearance caused by the addition or removal of helical turns in topologically closed double-stranded DNA.

DNA writhe

This approximates to our intuitive sense of DNA supercoiling. When helical turns are added to or subtracted from relaxed DNA, the DNA adopts a minimum energy state by winding the helical axis about itself.

Duplex slithering

In the absence of constraints (for example, due to protein binding), the DNA duplex is free to migrate in the plectonemically interwound, supercoiled structure by adopting a slithering motion.

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Dillon, S., Dorman, C. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8, 185–195 (2010). https://doi.org/10.1038/nrmicro2261

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