Dynamics of bacterial operons during genome-wide stresses are influenced by premature terminations and internal promoters

Bacterial gene networks have many operons, each coordinating a few genes.
In Escherichia coli, half of the operons have internal promoters
regulating downstream genes independently from upstream genes. We studied
their role during genome-wide stresses targeting key transcription
regulators, RNAP, and gyrase. We show that the operons' stress
response dynamics are highly influenced by premature terminations of
transcription elongation and internal promoters (specifically, their
numbers, positioning, and responsiveness). Moreover, premature
terminations are influenced by positive supercoiling buildup, collisions
between elongating and promoter-bound RNAPs, and sequences commonly found
at 3’ ends of RNA. We report the same findings in E. coli cells subject to
other stresses and in the evolutionarily distant Bacillus subtilis,
Corynebacterium glutamicum, and Helicobacter pylori. Our results suggest
that the strength, number, and positioning of internal promoters in
operons are subject to evolutionary pressure by a genome-wide need to
compensate for premature terminations and provide distal genes in operons
similar response strengths as genes proximal to the primary promoter.