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

Abstract

Bacterial gene networks have operons, each coordinating several genes under a primary promoter. Half of the operons in <i>Escherichia coli</i> have been reported to also contain internal promoters. We studied their role during genome-wide stresses targeting key transcription regulators, RNA polymerase (RNAP) and gyrase. Our results suggest that operons' responses are influenced by stress-related changes in premature elongation terminations and internal promoters' activity. Globally, this causes the responses of genes in the same operon to differ with the distance between them in a wave-like pattern. Meanwhile, premature terminations are affected by positive supercoiling buildup, collisions between elongating and promoter-bound RNAPs, and local regulatory elements. We report similar findings in <i>E. coli</i> under other stresses and in evolutionarily distant bacteria <i>Bacillus subtilis</i>, <i>Corynebacterium glutamicum</i>, and <i>Helicobacter pylori</i>. Our results suggest that the strength, number, and positioning of operons' internal promoters might have evolved to compensate for premature terminations, providing distal genes similar response strengths.