A Qrr Noncoding RNA Deploys Four Different Regulatory Mechanisms to Optimize Quorum-Sensing Dynamics

• Published in: Cell 2015-01, Vol.160 (1-2), p.228-240
• Main Authors: Feng, Lihui, Rutherford, Steven T., Papenfort, Kai, Bagert, John D., van Kessel, Julia C., Tirrell, David A., Wingreen, Ned S., Bassler, Bonnie L.
• Format: Article
• Language: English
• Subjects: Base Sequence; Escherichia coli - genetics; Inverted Repeat Sequences; Molecular Sequence Data; Nucleic Acid Conformation; Quorum Sensing; RNA, Bacterial - chemistry; RNA, Bacterial - genetics; RNA, Bacterial - metabolism; RNA, Messenger - genetics; RNA, Messenger - metabolism; RNA, Small Untranslated - chemistry; RNA, Small Untranslated - genetics; RNA, Small Untranslated - metabolism; Vibrio - genetics; Vibrio - metabolism
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2014.11.051

Quorum sensing is a cell-cell communication process that bacteria use to transition between individual and social lifestyles. In vibrios, homologous small RNAs called the Qrr sRNAs function at the center of quorum-sensing pathways. The Qrr sRNAs regulate multiple mRNA targets including those encoding the quorum-sensing regulatory components luxR, luxO, luxM, and aphA. We show that a representative Qrr, Qrr3, uses four distinct mechanisms to control its particular targets: the Qrr3 sRNA represses luxR through catalytic degradation, represses luxM through coupled degradation, represses luxO through sequestration, and activates aphA by revealing the ribosome binding site while the sRNA itself is degraded. Qrr3 forms different base-pairing interactions with each mRNA target, and the particular pairing strategy determines which regulatory mechanism occurs. Combined mathematical modeling and experiments show that the specific Qrr regulatory mechanism employed governs the potency, dynamics, and competition of target mRNA regulation, which in turn, defines the overall quorum-sensing response. [Display omitted] •The Qrr sRNA uses four different mechanisms to regulate target mRNAs•Base-pairing patterns determine the particular sRNA regulatory mechanism•The different regulatory mechanisms confer distinct regulatory strength and dynamics•The particular regulatory mechanisms are crucial for overall quorum-sensing dynamics Five noncoding RNAs, called the Qrr sRNAs, control Vibrio harveyi quorum sensing. Here, we demonstrate that the Qrr sRNAs employ four different mechanisms to control target genes. The Qrr sRNAs repress luxR through catalytic degradation, repress luxM through coupled degradation, repress luxO through sequestration, and activate aphA by revealing the ribosome-binding site while the sRNAs themselves are degraded. Importantly, the particular mechanism used defines the precise dynamics of quorum-sensing outputs.