Structural Coupling between RNA Polymerase Composition and DNA Supercoiling in Coordinating Transcription: a Global Role for the Omega Subunit?

ABSTRACT In growing bacterial cells, the global reorganization of transcription is associated with alterations of RNA polymerase composition and the superhelical density of the DNA. However, the existence of any regulatory device coordinating these changes remains elusive. Here we show that in an exponentially growing Escherichia coli rpoZmutant lacking the polymerase subunit, the impact of the E38 holoenzyme on transcription is enhanced in parallel with overall DNA relaxation. Conversely, overproduction of70 in an rpoZmutant increases both overall DNA supercoiling and the transcription of genes utilizing high negative superhelicity. We further show that transcription driven by the E38 and E70 holoenzymes from cognate promoters induces distinct superhelical densities of plasmid DNA in vivo. We thus demonstrate a tight coupling between polymerase ho-loenzyme composition and the supercoiling regimen of genomic transcription. Accordingly, we identify functional clusters of genes with distinct factor and supercoiling preferences arranging alternative transcription programs sustaining bacterial ex-ponential growth.We propose that structural coupling between DNA topology and holoenzyme composition provides a basic regulatory device for coordinating genome-wide transcription during bacterial growth and adaptation. IMPORTANCE Understanding the mechanisms of coordinated gene expression is pivotal for developing knowledge-based ap-proaches to manipulating bacterial physiology, which is a problem of central importance for applications of biotechnology an