Home LiteratureArticle Details
PMID: 20188674 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Negative feedback loops involving small regulatory RNAs precisely control the Vibrio harveyi quorum-sensing response.

Molecular cell ·Vol. 37 ·No. 4 ·2010-02-26 ·Pages 567-79

Tu KC, Long T, Svenningsen SL, Wingreen NS, Bassler BL

Abstract

Quorum-sensing (QS) bacteria assess population density through secretion and detection of molecules called autoinducers (AIs). We identify and characterize two Vibrio harveyi negative feedback loops that facilitate precise transitions between low-cell-density (LCD) and high-cell-density (HCD) states. The QS central regulator LuxO autorepresses its own transcription, and the Qrr small regulatory RNAs (sRNAs) posttranscriptionally repress luxO. Disrupting feedback increases the concentration of AIs required for cells to transit from LCD to HCD QS modes. Thus, the two cooperative negative feedback loops determine the point at which V. harveyi has reached a quorum and control the range of AIs over which the transition occurs. Negative feedback regulation also constrains the range of QS output by preventing sRNA levels from becoming too high and preventing luxO mRNA levels from reaching zero. We suggest that sRNA-mediated feedback regulation is a network design feature that permits fine-tuning of gene regulation and maintenance of homeostasis.

MeSH Terms
Bacterial Proteins/genetics,metabolism Base Sequence Gene Expression Regulation, Bacterial Molecular Sequence Data Nucleic Acid Conformation Protein Biosynthesis Quorum Sensing RNA Processing, Post-Transcriptional RNA, Bacterial/chemistry,genetics,metabolism Repressor Proteins/genetics,metabolism Transcription, Genetic Vibrio/chemistry,genetics,metabolism
Chemicals
Bacterial Proteins LuxO protein, Vibrio harveyi RNA, Bacterial Repressor Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Tu Kimberly C
Department of Molecular Biology, Princeton University, Princeton, NJ 08544-1014, USA.
Long Tao
Svenningsen Sine L
Wingreen Ned S
Bassler Bonnie L
References (21)
21 references, click to expand
  1. Autoinduction and signal transduction in the regulation of staphylococcal virulence.
    Mol Microbiol. 2003 Jun;48(6):1429-49 PMID: 12791129
  2. The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers.
    Genes Dev. 2006 Oct 1;20(19):2754-67 PMID: 17015436
  3. Molecular biology of bacterial bioluminescence.
    Microbiol Rev. 1991 Mar;55(1):123-42 PMID: 2030669
  4. Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing.
    EMBO J. 2009 Feb 18;28(4):429-39 PMID: 19165149
  5. A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi.
    Mol Microbiol. 1999 Jan;31(2):665-77 PMID: 10027982
  6. Engineering stability in gene networks by autoregulation.
    Nature. 2000 Jun 1;405(6786):590-3 PMID: 10850721
  7. Comparison of classical and autogenous systems of regulation in inducible operons.
    Nature. 1974 Dec 13;252(5484):546-9 PMID: 4431516
  8. Developmental biology in marine invertebrate symbioses.
    Curr Opin Microbiol. 2000 Dec;3(6):603-7 PMID: 11121780
  9. Quantifying the integration of quorum-sensing signals with single-cell resolution.
    PLoS Biol. 2009 Mar 24;7(3):e68 PMID: 19320539
  10. Negative autoregulation linearizes the dose-response and suppresses the heterogeneity of gene expression.
    Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5123-8 PMID: 19279212
  11. Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi.
    Genes Dev. 2007 Jan 15;21(2):221-33 PMID: 17234887
  12. A small-RNA-mediated negative feedback loop controls quorum-sensing dynamics in Vibrio harveyi.
    Mol Microbiol. 2008 Nov;70(4):896-907 PMID: 18808382
  13. The luxR gene product of Vibrio harveyi is a transcriptional activator of the lux promoter.
    J Bacteriol. 1992 Nov;174(22):7490-3 PMID: 1385389
  14. The Vibrio harveyi master quorum-sensing regulator, LuxR, a TetR-type protein is both an activator and a repressor: DNA recognition and binding specificity at target promoters.
    Mol Microbiol. 2008 Oct;70(1):76-88 PMID: 18681939
  15. Negative autoregulation speeds the response times of transcription networks.
    J Mol Biol. 2002 Nov 8;323(5):785-93 PMID: 12417193
  16. Intrinsic noise in gene regulatory networks.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8614-9 PMID: 11438714
  17. Quorum sensing: cell-to-cell communication in bacteria.
    Annu Rev Cell Dev Biol. 2005;21:319-46 PMID: 16212498
  18. The involvement of cell-to-cell signals in the development of a bacterial biofilm.
    Science. 1998 Apr 10;280(5361):295-8 PMID: 9535661
  19. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae.
    Cell. 2004 Jul 9;118(1):69-82 PMID: 15242645
  20. Gene regulation at the single-cell level.
    Science. 2005 Mar 25;307(5717):1962-5 PMID: 15790856
  21. Proximal and distal sites bind LuxR independently and activate expression of the Vibrio harveyi lux operon.
    Mol Microbiol. 1994 Oct;14(2):255-62 PMID: 7830570
Article Info
Journal
Molecular cell
Abbr.
Mol Cell
ISSN
1097-4164
Published
2010-02-26
Pages
567-79
Language
English
Region
United States
NLM ID
9802571
PMCID
PMC2844700
Subset
IM
Grants
NIGMS NIH HHS · R01 GM065859 · United States
NIAID NIH HHS · 5R01AI054442 · United States
NIAID NIH HHS · R01 AI054442 · United States
NIGMS NIH HHS · R01 GM065859-07 · United States
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · 5R01GM065859 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]