Quorum-sensing

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Annu. Rev. Genet. 2001. 35:439–68 Copyright c 2001 by Annual Reviews. All rights reserved

REGULATION OF GENE EXPRESSION BY CELL-TO-CELL COMMUNICATION:
Acyl-Homoserine Lactone Quorum Sensing
Clay Fuqua1, Matthew R. Parsek2, and E. Peter Greenberg3
1

Department of Biology, Indiana University, Bloomington, Indiana 47405; e-mail: cfuqua@bio.indiana.edu; 2Department of Civil Engineering,Northwestern University, Evanston, Illinois 60208; e-mail: m-parsek@nwu.edu; 3Department of Microbiology, University of Iowa, Iowa City, Iowa 52242; e-mail: everett-greenberg@uiowa.edu

Key Words quorum sensing, acylated homoserine lactones, intercellular signaling, bacterial communication, multicellularity s Abstract Quorum sensing is an example of community behavior prevalent among diversebacterial species. The term “quorum sensing” describes the ability of a microorganism to perceive and respond to microbial population density, usually relying on the production and subsequent response to diffusible signal molecules. A significant number of gram-negative bacteria produce acylated homoserine lactones (acyl-HSLs) as signal molecules that function in quorum sensing. Bacteria that produceacyl-HSLs can respond to the local concentration of the signaling molecules, and high population densities foster the accumulation of inducing levels of acyl-HSLs. Depending upon the bacterial species, the physiological processes regulated by quorum sensing are extremely diverse, ranging from bioluminescence to swarming motility. Acyl-HSL quorum sensing has become a paradigm for intercellularsignaling mechanisms. A flurry of research over the past decade has led to significant understanding of many aspects of quorum sensing including the synthesis of acyl-HSLs, the receptors that recognize the acyl-HSL signal and transduce this information to the level of gene expression, and the interaction of these receptors with the transcriptional machinery. Recent studies have begun to integrate acyl-HSLquorum sensing into global regulatory networks and establish its role in developing and maintaining the structure of bacterial communities. CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . QUORUM SENSING IN THE REAL WORLD: ENVIRONMENTAL CONSIDERATIONS . . . . . . . . . . . . . . . . . . . . . . . . MOLECULAR MECHANISMSOF QUORUM SENSING . . . . . . . . . . . . . . . . . . . . Acyl-HSL Structures and Synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . LuxI-Type Acyl-HSL Synthases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dynamics of Acyl-HSL Accumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .0066-4197/01/1215-0439$14.00 440 442 443 443 445 449

439

440

FUQUA

PARSEK

GREENBERG 450 456 458 460

LuxR-Type Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Modulation of Quorum Sensing Through Regulatory Gene Expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Fine Tuning of Quorum Sensing . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . PERSPECTIVE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

INTRODUCTION
A few words are necessary on the mass-action of bacteria. It is a common observation, one made by the writer at least a hundred times, that in culturemedia not exactly adapted to theneeds of the organism, a scanty inoculation may not give any growth—not even after a long time—whereas a copious one will lead to a growth which gradually clouds the fluid or covers the solid. The penetration of bacterial strands from cell to cell in the root nodules of Leguminosae is another example. The only explanation I can think of is that a multitude of bacteria are stronger than a few, and...
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