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

Feng, Lihui and Rutherford, Steven T. and Papenfort, Kai and Bagert, John D. and van Kessel, Julia C. and Tirrell, David A. and Wingreen, Ned S. and Bassler, Bonnie L. (2015) A Qrr Noncoding RNA Deploys Four Different Regulatory Mechanisms to Optimize Quorum-Sensing Dynamics. Cell, 160 (1-2). pp. 228-240. ISSN 0092-8674. PMCID PMC4313533. https://resolver.caltech.edu/CaltechAUTHORS:20150120-132939806

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Abstract

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.cell.2014.11.051DOIArticle
http://www.sciencedirect.com/science/article/pii/S0092867414015694PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4313533PubMed CentralArticle
ORCID:
AuthorORCID
Tirrell, David A.0000-0003-3175-4596
Additional Information:© 2015 Elsevier Inc. Received 2 May 2014, Revised 20 September 2014, Accepted 14 November 2014, Available online 8 January 2015. We thank Terence Hwa for generously providing the BW-RI strain and the pZA31-lucNB and pZE12G plasmids. We are indebted to members of the B.L.B. and N.S.W. laboratories for insightful discussions and suggestions. This work was supported by the Howard Hughes Medical Institute, NIH grant 5R01GM065859 and National Science Foundation (NSF) grant MCB-0343821 to B.L.B., NIH grant R01GM082938 to N.S.W., and NIH grant R01GM062523 and the Institute for Collaborative Biotechnologies through grant W911NF-09-0001 from the U.S. Army Research Office to D.A.T. K.P. is supported by a postdoctoral fellowship from the Human Frontiers in Science Program (HFSP). S.T.R. was supported by NIH fellowship F32AI085922. J.C.V.K. is supported by funds from Indiana University.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIH5R01GM065859
NSFMCB-0343821
NSFR01GM082938
NIHR01GM062523
Army Research Office (ARO)W911NF-09-0001
Human Frontiers in Science Program (HFSP) postdoctoral fellowshipUNSPECIFIED
NIH fellowshipF32AI085922
Indiana UniversityUNSPECIFIED
Issue or Number:1-2
PubMed Central ID:PMC4313533
Record Number:CaltechAUTHORS:20150120-132939806
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20150120-132939806
Official Citation:Lihui Feng, Steven T. Rutherford, Kai Papenfort, John D. Bagert, Julia C. van Kessel, David A. Tirrell, Ned S. Wingreen, Bonnie L. Bassler, A Qrr Noncoding RNA Deploys Four Different Regulatory Mechanisms to Optimize Quorum-Sensing Dynamics, Cell, Volume 160, Issues 1–2, 15 January 2015, Pages 228-240, ISSN 0092-8674, http://dx.doi.org/10.1016/j.cell.2014.11.051. (http://www.sciencedirect.com/science/article/pii/S0092867414015694)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:53888
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:20 Jan 2015 22:08
Last Modified:03 Oct 2019 07:53

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