Quorum-sensing-dependent regulation of staphylococcal virulence and biofilm development

When living in biological and interactive communities, microorganisms use quorum-sensing mechanisms for their communication. According to cell density, bacteria and fungi can produce signaling molecules (e.g., secondary metabolites), which participate, for example, in the regulation of gene expression and coordination of collective behavior in their natural niche. The existence of these secondary metabolites plays a main role in competence, colonization of host tissues and surfaces, morphogenesis, and biofilm development. Therefore, for the design of new antibacterials or antifungals and understanding on how these mechanisms occur, to inhibit the secretion of quorum-sensing (e.g., farnesol and tyrosol) molecules leading the progress of microbial infections seems to be an interesting option. In yeasts, farnesol has a main role in the morphological transition, inhibiting hyphae production in a concentration-dependent manner, while tyrosol has a contrary function, stimulating transition from spherical cells to germ tube form. It is beyond doubt that secretion of both molecules by fungi has not been fully described, but specific meaning for their existence has been found. This brief review summarizes the important function of these two compounds as signaling chemicals participating mainly in Candida morphogenesis and regulatory mechanisms.

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Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.170283397 ◽

2000 ◽

Vol 97 (17) ◽

pp. 9636-9641 ◽

Cited By ~ 224

Author(s):

M. H. Rashid ◽

K. Rumbaugh ◽

L. Passador ◽

D. G. Davies ◽

A. N. Hamood ◽

...

Keyword(s):

Pseudomonas Aeruginosa ◽

Quorum Sensing ◽

Polyphosphate Kinase ◽

Biofilm Development

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Quorum Sensing Influences Burkholderia thailandensis Biofilm Development and Matrix Production

Journal of Bacteriology ◽

10.1128/jb.00047-16 ◽

2016 ◽

Vol 198 (19) ◽

pp. 2643-2650 ◽

Cited By ~ 23

Author(s):

Boo Shan Tseng ◽

Charlotte D. Majerczyk ◽

Daniel Passos da Silva ◽

Josephine R. Chandler ◽

E. Peter Greenberg ◽

...

Keyword(s):

Quorum Sensing ◽

Biofilm Formation ◽

Bacterial Species ◽

Matrix Material ◽

Close Relative ◽

Wild Type ◽

Flow Conditions ◽

Burkholderia Thailandensis ◽

Content Type ◽

Biofilm Development

ABSTRACTMembers of the genusBurkholderiaare known to be adept at biofilm formation, which presumably assists in the survival of these organisms in the environment and the host. Biofilm formation has been linked to quorum sensing (QS) in several bacterial species. In this study, we characterizedBurkholderia thailandensisbiofilm development under flow conditions and sought to determine whether QS contributes to this process.B. thailandensisbiofilm formation exhibited an unusual pattern: the cells formed small aggregates and then proceeded to produce mature biofilms characterized by “dome” structures filled with biofilm matrix material. We showed that this process was dependent on QS.B. thailandensishas three acyl-homoserine lactone (AHL) QS systems (QS-1, QS-2, and QS-3). An AHL-negative strain produced biofilms consisting of cell aggregates but lacking the matrix-filled dome structures. This phenotype was rescued via exogenous addition of the three AHL signals. Of the threeB. thailandensisQS systems, we show that QS-1 is required for proper biofilm development, since abtaR1mutant, which is defective in QS-1 regulation, forms biofilms without these dome structures. Furthermore, our data show that the wild-type biofilm biomass, as well as the material inside the domes, stains with a fucose-binding lectin. ThebtaR1mutant biofilms, however, are negative for fucose staining. This suggests that the QS-1 system regulates the production of a fucose-containing exopolysaccharide in wild-type biofilms. Finally, we present data showing that QS ability during biofilm development produces a biofilm that is resistant to dispersion under stress conditions.IMPORTANCEThe saprophyteBurkholderia thailandensisis a close relative of the pathogenic bacteriumBurkholderia pseudomallei, the causative agent of melioidosis, which is contracted from its environmental reservoir. Since most bacteria in the environment reside in biofilms,B. thailandensisis an ideal model organism for investigating questions inBurkholderiaphysiology. In this study, we characterizedB. thailandensisbiofilm development and sought to determine if quorum sensing (QS) contributes to this process. Our work shows thatB. thailandensisproduces biofilms with unusual dome structures under flow conditions. Our findings suggest that these dome structures are filled with a QS-regulated, fucose-containing exopolysaccharide that may be involved in the resilience ofB. thailandensisbiofilms against changes in the nutritional environment.

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Quorum-Sensing Genes in Pseudomonas aeruginosa Biofilms: Their Role and Expression Patterns

Applied and Environmental Microbiology ◽

10.1128/aem.67.4.1865-1873.2001 ◽

2001 ◽

Vol 67 (4) ◽

pp. 1865-1873 ◽

Cited By ~ 341

Author(s):

Teresa R. De Kievit ◽

Richard Gillis ◽

Steve Marx ◽

Chris Brown ◽

Barbara H. Iglewski

Keyword(s):

Pseudomonas Aeruginosa ◽

Quorum Sensing ◽

Biofilm Formation ◽

Fluorescent Protein ◽

Expression Patterns ◽

Homoserine Lactone ◽

Lower Percentage ◽

Spatial Studies ◽

Green Fluorescent ◽

Biofilm Development

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). InPseudomonas 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 andrhlI 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 andrhlI 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.

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Screening for Quorum-Sensing Inhibitors (QSI) by Use of a Novel Genetic System, the QSI Selector

Journal of Bacteriology ◽

10.1128/jb.187.5.1799-1814.2005 ◽

2005 ◽

Vol 187 (5) ◽

pp. 1799-1814 ◽

Cited By ~ 398

Author(s):

Thomas Bovbjerg Rasmussen ◽

Thomas Bjarnsholt ◽

Mette Elena Skindersoe ◽

Morten Hentzer ◽

Peter Kristoffersen ◽

...

Keyword(s):

Quorum Sensing ◽

Genetic System ◽

Garlic Extract ◽

Resistant Bacteria ◽

Antimicrobial Drugs ◽

Synthetic Compound ◽

Compound Libraries ◽

Promising Target ◽

Increasing Demand ◽

Biofilm Development

ABSTRACT With the widespread appearance of antibiotic-resistant bacteria, there is an increasing demand for novel strategies to control infectious diseases. Furthermore, it has become apparent that the bacterial life style also contributes significantly to this problem. Bacteria living in the biofilm mode of growth tolerate conventional antimicrobial treatments. The discovery that many bacteria use quorum-sensing (QS) systems to coordinate virulence and biofilm development has pointed out a new, promising target for antimicrobial drugs. We constructed a collection of screening systems, QS inhibitor (QSI) selectors, which enabled us to identify a number of novel QSIs among natural and synthetic compound libraries. The two most active were garlic extract and 4-nitro-pyridine-N-oxide (4-NPO). GeneChip-based transcriptome analysis revealed that garlic extract and 4-NPO had specificity for QS-controlled virulence genes in Pseudomonas aeruginosa. These two QSIs also significantly reduced P. aeruginosa biofilm tolerance to tobramycin treatment as well as virulence in a Caenorhabditis elegans pathogenesis model.

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Microarray Analysis of Pseudomonas aeruginosa Quorum-Sensing Regulons: Effects of Growth Phase and Environment

Journal of Bacteriology ◽

10.1128/jb.185.7.2080-2095.2003 ◽

2003 ◽

Vol 185 (7) ◽

pp. 2080-2095 ◽

Cited By ~ 627

Author(s):

Victoria E. Wagner ◽

Daniel Bushnell ◽

Luciano Passador ◽

Andrew I. Brooks ◽

Barbara H. Iglewski

Keyword(s):

Pseudomonas Aeruginosa ◽

Quorum Sensing ◽

Expression Patterns ◽

Antibiotic Sensitivity ◽

Opportunistic Pathogen ◽

Homoserine Lactone ◽

Medium Composition ◽

Logarithmic Phase ◽

Significant Differential Expression ◽

Biofilm Development

ABSTRACT Bacterial communication via quorum sensing (QS) has been reported to be important in the production of virulence factors, antibiotic sensitivity, and biofilm development. Two QS systems, known as the las and rhl systems, have been identified previously in the opportunistic pathogen Pseudomonas aeruginosa. High-density oligonucleotide microarrays for the P. aeruginosa PAO1 genome were used to investigate global gene expression patterns modulated by QS regulons. In the initial experiments we focused on identifying las and/or rhl QS-regulated genes using a QS signal generation-deficient mutant (PAO-JP2) that was cultured with and without added exogenous autoinducers [N-(3-oxododecanoyl) homoserine lactone and N-butyryl homoserine lactone]. Conservatively, 616 genes showed statistically significant differential expression (P ≤ 0.05) in response to the exogenous autoinducers and were classified as QS regulated. A total of 244 genes were identified as being QS regulated at the mid-logarithmic phase, and 450 genes were identified as being QS regulated at the early stationary phase. Most of the previously reported QS-promoted genes were confirmed, and a large number of additional QS-promoted genes were identified. Importantly, 222 genes were identified as being QS repressed. Environmental factors, such as medium composition and oxygen availability, eliminated detection of transcripts of many genes that were identified as being QS regulated.

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Involvement of quorum sensing genes in biofilm development and degradation of polycyclic aromatic hydrocarbons by a marine bacterium Pseudomonas aeruginosa N6P6

Applied Microbiology and Biotechnology ◽

10.1007/s00253-015-6868-7 ◽

2015 ◽

Vol 99 (23) ◽

pp. 10283-10297 ◽

Cited By ~ 35

Author(s):

Neelam Mangwani ◽

Supriya Kumari ◽

Surajit Das

Keyword(s):

Pseudomonas Aeruginosa ◽

Polycyclic Aromatic Hydrocarbons ◽

Quorum Sensing ◽

Aromatic Hydrocarbons ◽

Marine Bacterium ◽

Polycyclic Aromatic ◽

Biofilm Development

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Mechanistic understanding of Phenyllactic acid mediated inhibition of quorum sensing and biofilm development in Pseudomonas aeruginosa

Applied Microbiology and Biotechnology ◽

10.1007/s00253-017-8546-4 ◽

2017 ◽

Vol 101 (22) ◽

pp. 8223-8236 ◽

Cited By ~ 23

Author(s):

Maitrayee Chatterjee ◽

Sharon D’Morris ◽

Vinod Paul ◽

Sruthi Warrier ◽

Anil Kumar Vasudevan ◽

...

Keyword(s):

Pseudomonas Aeruginosa ◽

Quorum Sensing ◽

Phenyllactic Acid ◽

Mechanistic Understanding ◽

Biofilm Development

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Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm

Journal of Bacteriology ◽

10.1128/jb.184.4.1140-1154.2002 ◽

2002 ◽

Vol 184 (4) ◽

pp. 1140-1154 ◽

Cited By ~ 1026

Author(s):

Karin Sauer ◽

Anne K. Camper ◽

Garth D. Ehrlich ◽

J. William Costerton ◽

David G. Davies

Keyword(s):

Pseudomonas Aeruginosa ◽

Quorum Sensing ◽

Protein Identification ◽

Electrophoretic Analysis ◽

Cell Protein ◽

Biofilm Growth ◽

Alginate Production ◽

Multiple Phenotypes ◽

Reporter Gene Analysis ◽

Biofilm Development

ABSTRACT Complementary approaches were employed to characterize transitional episodes in Pseudomonas aeruginosa biofilm development using direct observation and whole-cell protein analysis. Microscopy and in situ reporter gene analysis were used to directly observe changes in biofilm physiology and to act as signposts to standardize protein collection for two-dimensional electrophoretic analysis and protein identification in chemostat and continuous-culture biofilm-grown populations. Using these approaches, we characterized five stages of biofilm development: (i) reversible attachment, (ii) irreversible attachment, (iii) maturation-1, (iv) maturation-2, and (v) dispersion. Biofilm cells were shown to change regulation of motility, alginate production, and quorum sensing during the process of development. The average difference in detectable protein regulation between each of the five stages of development was 35% (approximately 525 proteins). When planktonic cells were compared with maturation-2 stage biofilm cells, more than 800 proteins were shown to have a sixfold or greater change in expression level (over 50% of the proteome). This difference was higher than when planktonic P. aeruginosa were compared with planktonic cultures of Pseudomonas putida. Las quorum sensing was shown to play no role in early biofilm development but was important in later stages. Biofilm cells in the dispersion stage were more similar to planktonic bacteria than to maturation-2 stage bacteria. These results demonstrate that P. aeruginosa displays multiple phenotypes during biofilm development and that knowledge of stage-specific physiology may be important in detecting and controlling biofilm growth.

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