Two quorum sensing systems control biofilm formation and virulence in members of theBurkholderia cepaciacomplex

ABSTRACT Vibrio cholerae, the pathogen that causes cholera, also survives in aqueous reservoirs, probably in the form of biofilms. Quorum sensing negatively regulates V. cholerae biofilm formation through HapR, whose expression is induced at a high cell density. In this study, we show that the concentration of the quorum-sensing signal molecule CAI-1 is higher in biofilms than in planktonic cultures. By measuring hapR expression and activity, we found that the induction of quorum sensing in biofilm-associated cells occurs earlier. We further demonstrate that the timing of hapR expression is crucial for biofilm thickness, biofilm detachment rates, and intestinal colonization efficiency. These results suggest that V. cholerae is able to regulate its biofilm architecture by temporal induction of quorum-sensing systems.

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Quorum-Sensing Systems in the Plant Growth-Promoting Bacterium Paraburkholderia phytofirmans PsJN Exhibit Cross-Regulation and Are Involved in Biofilm Formation

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-01-17-0008-r ◽

2017 ◽

Vol 30 (7) ◽

pp. 557-565 ◽

Cited By ~ 16

Author(s):

Ana Zúñiga ◽

Raúl A. Donoso ◽

Daniela Ruiz ◽

Gonzalo A. Ruz ◽

Bernardo González

Keyword(s):

Quorum Sensing ◽

Biofilm Formation ◽

Type Strain ◽

Wild Type Strain ◽

Homoserine Lactone ◽

Wild Type ◽

Transcript Levels ◽

Sensing Systems ◽

Plant Growth Promoting ◽

Growth Promoting

Quorum-sensing systems play important roles in host colonization and host establishment of Burkholderiales species. Beneficial Paraburkholderia species share a conserved quorum-sensing (QS) system, designated BraI/R, that controls different phenotypes. In this context, the plant growth-promoting bacterium Paraburkholderia phytofirmans PsJN possesses two different homoserine lactone QS systems BpI.1/R.1 and BpI.2/R.2 (BraI/R-like QS system). The BpI.1/R.1 QS system was previously reported to be important to colonize and produce beneficial effects in Arabidopsis thaliana plants. Here, we analyzed the temporal variations of the QS gene transcript levels in the wild-type strain colonizing plant roots. The gene expression patterns showed relevant differences in both QS systems compared with the wild-type strain in the unplanted control treatment. The gene expression data were used to reconstruct a regulatory network model of QS systems in P. phytofirmans PsJN, using a Boolean network model. Also, we examined the phenotypic traits and transcript levels of genes involved in QS systems, using P. phytofirmans mutants in homoserine lactone synthases genes. We observed that the BpI.1/R.1 QS system regulates biofilm formation production in strain PsJN and this phenotype was associated with the lower expression of a specific extracytoplasmic function sigma factor ecf26.1 gene (implicated in biofilm formation) in the bpI.1 mutant strain.

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Inhibition of Quorum Sensing in Pseudomonas aeruginosa by N-Acyl Cyclopentylamides

Applied and Environmental Microbiology ◽

10.1128/aem.02233-06 ◽

2007 ◽

Vol 73 (10) ◽

pp. 3183-3188 ◽

Cited By ~ 114

Author(s):

Takenori Ishida ◽

Tsukasa Ikeda ◽

Noboru Takiguchi ◽

Akio Kuroda ◽

Hisao Ohtake ◽

...

Keyword(s):

Pseudomonas Aeruginosa ◽

Quorum Sensing ◽

Virulence Factors ◽

Biofilm Formation ◽

Homoserine Lactone ◽

Ring Structure ◽

Response Regulators ◽

Maximal Inhibition ◽

Sensing Systems ◽

Reporter Assays

ABSTRACT N-Octanoyl cyclopentylamide (C8-CPA) was found to moderately inhibit quorum sensing in Pseudomonas aeruginosa PAO1. To obtain more powerful inhibitors, a series of structural analogs of C8-CPA were synthesized and examined for their ability to inhibit quorum sensing in P. aeruginosa PAO1. The lasB-lacZ and rhlA-lacZ reporter assays revealed that the chain length and the ring structure were critical for C8-CPA analogs to inhibit quorum sensing. N-Decanoyl cyclopentylamide (C10-CPA) was found to be the strongest inhibitor, and its concentrations required for half-maximal inhibition for lasB-lacZ and rhlA-lacZ expression were 80 and 90 μM, respectively. C10-CPA also inhibited production of virulence factors, including elastase, pyocyanin, and rhamnolipid, and biofilm formation without affecting growth of P. aeruginosa PAO1. C10-CPA inhibited induction of both lasI-lacZ by N-(3-oxododecanoyl)-l-homoserine lactone (PAI1) and rhlA-lacZ by N-butanoyl-l-homoserine lactone (PAI2) in the lasI rhlI mutant of P. aeruginosa PAO1, indicating that C10-CPA interferes with the las and rhl quorum-sensing systems via inhibiting interaction between their response regulators (LasR and RhlR) and autoinducers.

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N-Octanoylhomoserine lactone signalling mediated by the BpsI–BpsR quorum sensing system plays a major role in biofilm formation of Burkholderia pseudomallei

Microbiology ◽

10.1099/mic.0.046540-0 ◽

2011 ◽

Vol 157 (4) ◽

pp. 1176-1186 ◽

Cited By ~ 37

Author(s):

Akshamal Mihiranga Gamage ◽

Guanghou Shui ◽

Markus R. Wenk ◽

Kim Lee Chua

Keyword(s):

Quorum Sensing ◽

Biofilm Formation ◽

Burkholderia Pseudomallei ◽

Homoserine Lactone ◽

Tandem Ms ◽

Wild Type ◽

Acylhomoserine Lactone ◽

Sensing System ◽

Sensing Systems ◽

Quorum Sensing System

The genome of Burkholderia pseudomallei encodes three acylhomoserine lactone (AHL) quorum sensing systems, each comprising an AHL synthase and a signal receptor/regulator. The BpsI–BpsR system produces N-octanoylhomoserine lactone (C8HL) and is positively auto-regulated by its AHL product. The products of the remaining two systems have not been identified. In this study, tandem MS was used to identify and quantify the AHL species produced by three clinical B. pseudomallei isolates – KHW, K96243 and H11 – three isogenic KHW mutants that each contain a null mutation in an AHL synthase gene, and recombinant Escherichia coli heterologously expressing each of the three B. pseudomallei AHL synthase genes. BpsI synthesized predominantly C8HL, which accounted for more than 95 % of the extracellular AHLs produced in stationary-phase KHW cultures. The major products of BpsI2 and BpsI3 were N-(3-hydroxy-octanoyl)homoserine lactone (OHC8HL) and N-(3-hydroxy-decanoyl)homoserine lactone, respectively, and their corresponding transcriptional regulators, BpsR2 and BpsR3, were capable of driving reporter gene expression in the presence of these cognate lactones. Formation of biofilm by B. pseudomallei KHW was severely impaired in mutants lacking either BpsI or BpsR but could be restored to near wild-type levels by exogenous C8HL. BpsI2 was not required, and BpsI3 was partially required for biofilm formation. Unlike the bpsI mutant, biofilm formation in the bpsI3 mutant could not be restored to wild-type levels in the presence of OHC8HL, the product of BpsI3. C8HL and OHC8HL had opposite effects on biofilm formation; exogenous C8HL enhanced biofilm formation in both the bpsI3 mutant and wild-type KHW while exogenous OHC8HL suppressed the formation of biofilm in the same strains. We propose that exogenous OHC8HL antagonizes biofilm formation in B. pseudomallei, possibly by competing with endogenous C8HL for binding to BpsR.

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Presence of Quorum-sensing Systems Associated with Multidrug Resistance and Biofilm Formation in Bacteroides fragilis

Microbial Ecology ◽

10.1007/s00248-007-9358-3 ◽

2008 ◽

Vol 56 (3) ◽

pp. 412-419 ◽

Cited By ~ 38

Author(s):

Lilian Pumbwe ◽

Christopher A. Skilbeck ◽

Hannah M. Wexler

Keyword(s):

Multidrug Resistance ◽

Quorum Sensing ◽

Biofilm Formation ◽

Bacteroides Fragilis ◽

Sensing Systems

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Quorum sensing systems, related virulence factors, and biofilm formation in Pseudomonas aeruginosa isolated from fish

Archives of Microbiology ◽

10.1007/s00203-020-02159-5 ◽

2021 ◽

Author(s):

Belgin Sırıken ◽

Veli Öz ◽

İrfan Erol

Keyword(s):

Pseudomonas Aeruginosa ◽

Quorum Sensing ◽

Virulence Factors ◽

Biofilm Formation ◽

Sensing Systems

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Characterisation of two quorum sensing systems in the endophytic Serratia plymuthica strain G3: differential control of motility and biofilm formation according to life-style

BMC Microbiology ◽

10.1186/1471-2180-11-26 ◽

2011 ◽

Vol 11 (1) ◽

pp. 26 ◽

Cited By ~ 44

Author(s):

Xiaoguang Liu ◽

Jinli Jia ◽

Roman Popat ◽

Catherine A Ortori ◽

Jun Li ◽

...

Keyword(s):

Quorum Sensing ◽

Life Style ◽

Biofilm Formation ◽

Serratia Plymuthica ◽

Sensing Systems ◽

Differential Control

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CRISPR-cas3 of Salmonella Upregulates Bacterial Biofilm Formation and Virulence to Host Cells by Targeting Quorum-Sensing Systems

Pathogens ◽

10.3390/pathogens9010053 ◽

2020 ◽

Vol 9 (1) ◽

pp. 53 ◽

Cited By ~ 6

Author(s):

Luqing Cui ◽

Xiangru Wang ◽

Deyu Huang ◽

Yue Zhao ◽

Jiawei Feng ◽

...

Keyword(s):

Quorum Sensing ◽

Biofilm Formation ◽

Bacterial Biofilm ◽

Host Cells ◽

Microbial Pathogens ◽

Bacterial Invasion ◽

Type I ◽

Salmonella Enterica Serovar Enteritidis ◽

Sensing Systems ◽

Type Three Secretion System

Salmonella is recognized as one of the most common microbial pathogens worldwide. The bacterium contains the clustered regularly interspaced short palindromic repeats (CRISPR)-CRISPR-associated (Cas) systems, providing adaptive immunity against invading foreign nucleic acids. Previous studies suggested that certain bacteria employ the Cas proteins of CRISPR-Cas systems to target their own genes, which also alters the virulence during invasion of mammals. However, whether CRISPR-Cas systems in Salmonella have similar functions during bacterial invasion of host cells remains unknown. Here, we systematically analyzed the genes that are regulated by Cas3 in a type I-E CRISPR-Cas system and the virulence changes due to the deletion of cas3 in Salmonella enterica serovar Enteritidis. Compared to the cas3 gene wild-type (cas3 WT) Salmonella strain, cas3 deletion upregulated the lsrFGBE genes in lsr (luxS regulated) operon related to quorum sensing (QS) and downregulated biofilm-forming-related genes and Salmonella pathogenicity island 1 (SPI-1) genes related to the type three secretion system (T3SS). Consistently, the biofilm formation ability was downregulated in the cas3 deletion mutant (Δcas3). The bacterial invasive and intracellular capacity of Δcas3 to host cells was also reduced, thereby increasing the survival of infected host cells and live chickens. By the transcriptome-wide screen (RNA-Seq), we found that the cas3 gene impacts a series of genes related to QS, the flagellum, and SPI-1-T3SS system, thereby altering the virulence phenotypes. As QS SPI-1-T3SS and CRISPR-Cas systems are widely distributed in the bacteria kingdom, our findings extend our understanding of virulence regulation and pathogenicity in mammalian hosts for Salmonella and potentially other bacteria.

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