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Species-specific supercoil dynamics of the bacterial nucleoid

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Abstract

Bacteria organize DNA into self-adherent conglomerates called nucleoids that are replicated, transcribed, and partitioned within the cytoplasm during growth and cell division. Three classes of proteins help condense nucleoids: (1) DNA gyrase generates diffusible negative supercoils that help compact DNA into a dynamic interwound and multiply branched structure; (2) RNA polymerase and abundant small basic nucleoid-associated proteins (NAPs) create constrained supercoils by binding, bending, and forming cooperative protein–DNA complexes; (3) a multi-protein DNA condensin organizes chromosome structure to assist sister chromosome segregation after replication. Most bacteria have four topoisomerases that participate in DNA dynamics during replication and transcription. Gyrase and topoisomerase I (Topo I) are intimately involved in transcription; Topo III and Topo IV play critical roles in decatenating and unknotting DNA during and immediately after replication. RNA polymerase generates positive (+) supercoils downstream and negative (−) supercoils upstream of highly transcribed operons. Supercoil levels vary under fast versus slow growth conditions, but what surprises many investigators is that it also varies significantly between different bacterial species. The MukFEB condensin is dispensable in the high supercoil density (σ) organism Escherichia coli but is essential in Salmonella spp. which has 15 % fewer supercoils. These observations raise two questions: (1) How do different species regulate supercoil density? (2) Why do closely related species evolve different optimal supercoil levels? Control of supercoil density in E. coli and Salmonella is largely determined by differences encoded within the gyrase subunits. Supercoil differences may arise to minimalize toxicity of mobile DNA elements in the genome.

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Acknowledgments

Work in the Higgins lab has been supported by the United States National Institutes of Health grant GM-33143.

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Correspondence to N. Patrick Higgins.

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This article is part of a Special Issue on ‘DNA supercoiling, protein interactions and genetic function’ edited by Laura Finzi and Wilma Olson.

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Higgins, N.P. Species-specific supercoil dynamics of the bacterial nucleoid. Biophys Rev 8 (Suppl 1), 113–121 (2016). https://doi.org/10.1007/s12551-016-0207-9

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