Abstract
Acylated homoserine lactone molecules are used by a number of gram-negative bacteria to regulate cell density-dependent gene expression by a mechanism known as quorum sensing (QS). In Pseudomonas aeruginosa, QS or cell-to-cell signaling controls expression of a number of virulence factors, as well as biofilm differentiation. In this study, we investigated the role played by the las and rhl QS systems during the early stages of static biofilm formation when cells are adhering to a surface and forming microcolonies. These studies revealed a marked difference in biofilm formation between the PAO1 parent and the QS mutants when glucose, but not citrate, was used as the sole carbon source. To further elucidate the contribution of lasI and rhlI to biofilm maturation, we utilized fusions to unstable green fluorescent protein in concert with confocal microscopy to perform real-time temporal and spatial studies of these genes in a flowing environment. During the course of 8-day biofilm development, lasI expression was found to progressively decrease over time. Conversely, rhlI expression remained steady throughout biofilm development but occurred in a lower percentage of cells. Spatial analysis revealed that lasI and rhlI were maximally expressed in cells located at the substratum and that expression decreased with increasing biofilm height. Because QS was shown previously to be involved in biofilm differentiation, these findings have important implications for the design of biofilm prevention and eradication strategies.
MeSH Terms
Bacterial Proteins/genetics,metabolism
Biofilms/growth & development
Culture Media
Flagella/physiology
Gene Expression Regulation, Bacterial
Green Fluorescent Proteins
Image Processing, Computer-Assisted
Ligases
Lipopolysaccharides/metabolism
Luminescent Proteins/genetics,metabolism
Microscopy, Confocal
Pseudomonas aeruginosa/genetics,growth & development
Signal Transduction
Transcription Factors/genetics,metabolism
Chemicals
Bacterial Proteins
Culture Media
LasI protein, Pseudomonas aeruginosa
Lipopolysaccharides
Luminescent Proteins
Transcription Factors
Green Fluorescent Proteins
Ligases
RHLI protein, Pseudomonas aeruginosa
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
De Kievit T R
Department of Microbiology and Immunology, University of Rochester Medical Center, 601 Elmwood Ave., Rochester, NY 14642, USA.
Gillis R
Marx S
Brown C
Iglewski B H
References (21)
21 references, click to expand
-
Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family.
J Bacteriol. 1995 Dec;177(24):7155-63
PMID: 8522523
-
Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy.
J Bacteriol. 1995 Feb;177(3):654-9
PMID: 7836299
-
Functional analysis of the Pseudomonas aeruginosa autoinducer PAI.
J Bacteriol. 1996 Oct;178(20):5995-6000
PMID: 8830697
-
A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS.
Mol Microbiol. 1996 Sep;21(6):1137-46
PMID: 8898383
-
Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling.
J Bacteriol. 1996 Nov;178(22):6618-22
PMID: 8932319
-
Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa.
J Bacteriol. 1997 May;179(10):3127-32
PMID: 9150205
-
Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes.
J Bacteriol. 1997 Sep;179(18):5756-67
PMID: 9294432
-
Evidence of autoinducer activity in naturally occurring biofilms.
FEMS Microbiol Lett. 1997 Sep 15;154(2):259-63
PMID: 9311122
-
The involvement of cell-to-cell signals in the development of a bacterial biofilm.
Science. 1998 Apr 10;280(5361):295-8
PMID: 9535661
-
New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria.
Appl Environ Microbiol. 1998 Jun;64(6):2240-6
PMID: 9603842
-
Starvation selection restores elastase and rhamnolipid production in a Pseudomonas aeruginosa quorum-sensing mutant.
Infect Immun. 1998 Sep;66(9):4499-502
PMID: 9712807
-
Biofilms on indwelling urethral catheters produce quorum-sensing signal molecules in situ and in vitro.
Appl Environ Microbiol. 1998 Sep;64(9):3486-90
PMID: 9726901
-
Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development.
Mol Microbiol. 1998 Oct;30(2):295-304
PMID: 9791175
-
Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility.
J Bacteriol. 1999 Mar;181(5):1623-9
PMID: 10049396
-
Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa.
Microbiol Mol Biol Rev. 1999 Sep;63(3):523-53
PMID: 10477307
-
Molecular tools for study of biofilm physiology.
Methods Enzymol. 1999;310:20-42
PMID: 10547780
-
The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa.
J Bacteriol. 2000 Jan;182(2):425-31
PMID: 10629189
-
Chromosomal genetics of Pseudomonas.
Microbiol Rev. 1979 Mar;43(1):73-102
PMID: 111024
-
Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels.
J Bacteriol. 1983 Apr;154(1):269-77
PMID: 6187729
-
Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa.
Gene. 1994 Oct 11;148(1):81-6
PMID: 7926843
-
FACS-optimized mutants of the green fluorescent protein (GFP).
Gene. 1996;173(1 Spec No):33-8
PMID: 8707053