Abstract
We have investigated the connection between the four-dimensional architecture of the bacterial nucleoid and the organism's global gene expression programme. By localizing the transcription machinery and the transcriptional outputs across the genome of the model bacterium Salmonella enterica serovar Typhimurium at different stages of the growth cycle, a surprising disconnection between gene dosage and transcriptional output was revealed. During exponential growth, gene output occurred chiefly in the Ori (origin), Ter (terminus) and NSL (non-structured left) domains, whereas the Left macrodomain remained transcriptionally quiescent at all stages of growth. The apparently high transcriptional output in Ter was correlated with an enhanced stability of the RNA expressed there during exponential growth, suggesting that longer mRNA half-lives compensate for low gene dosage. During exponential growth, RNA polymerase (RNAP) was detected everywhere, whereas in stationary phase cells, RNAP was concentrated in the Ter macrodomain. The alternative sigma factors RpoE, RpoH and RpoN were not required to drive transcription in these growth conditions, consistent with their observed binding to regions away from RNAP and regions of active transcription. Specifically, these alternative sigma factors were found in the Ter macrodomain during exponential growth, whereas they were localized at the Ori macrodomain in stationary phase.
Highlights
IntroductionIt is becoming apparent that a blueprint for the gene expression programme of the cell may be written into the geography and architecture of the folded chromosome [1]
The bacterial chromosome is more than a carrier of genetic information
We examined the spatial distribution of genes encoding mRNA in multiple growth phases in the model pathogen S. enterica serovar Typhimurium
Summary
It is becoming apparent that a blueprint for the gene expression programme of the cell may be written into the geography and architecture of the folded chromosome [1]. This programme possesses both spatial and temporal dimensions, making it likely that the positions of genes within the genome, together with the timing of their expression, are important determinants of the programme’s operation [1, 2]. The chromosome of the model bacterium Salmonella enterica serovar Typhimurium has been studied for many decades as an aid to understanding the link between gene position and bacterial physiology [11,12,13,14,15,16,17]. An advantage of studies that focus on S. enterica serovar Typhimurium is that the chromosome of this pathogen is closely related in size, gene content and gene order to the chromosome of the commensal bacterium Escherichia coli, arguably the best 000127 ã 2017 The Authors
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