Bacterial quorum-sensing network architectures - PubMed
Review
Bacterial quorum-sensing network architectures
Wai-Leung Ng et al. Annu Rev Genet. 2009.
Abstract
Quorum sensing is a cell-cell communication process in which bacteria use the production and detection of extracellular chemicals called autoinducers to monitor cell population density. Quorum sensing allows bacteria to synchronize the gene expression of the group, and thus act in unison. Here, we review the mechanisms involved in quorum sensing with a focus on the Vibrio harveyi and Vibrio cholerae quorum-sensing systems. We discuss the differences between these two quorum-sensing systems and the differences between them and other paradigmatic bacterial signal transduction systems. We argue that the Vibrio quorum-sensing systems are optimally designed to precisely translate extracellular autoinducer information into internal changes in gene expression. We describe how studies of the V. harveyi and V. cholerae quorum-sensing systems have revealed some of the fundamental mechanisms underpinning the evolution of collective behaviors.
Figures

Structures of bacterial autoinducers. (A) Homoserine lactone autoinducers produced by different Gram-negative bacteria. (B) Amino acid sequences of three peptide autoinducers, ComX, CSF, and CSP, produced by Gram-positive bacteria. The underlined tryptophan in B. subtilis ComX is isoprenylated. The four different AIPs produced by S. aureus. (C) DPD, the precursor to AI-2. In the presence of boron, AI-2 exists as S-THMF-borate. In the absence of boron, AI-2 exists as R-THMF. (D) Structure of V. cholerae CAI-1 and Amino-CAI-1. (E) Structure of the PQS autoinducer of P. aeruginosa.

Structures of bacterial autoinducers. (A) Homoserine lactone autoinducers produced by different Gram-negative bacteria. (B) Amino acid sequences of three peptide autoinducers, ComX, CSF, and CSP, produced by Gram-positive bacteria. The underlined tryptophan in B. subtilis ComX is isoprenylated. The four different AIPs produced by S. aureus. (C) DPD, the precursor to AI-2. In the presence of boron, AI-2 exists as S-THMF-borate. In the absence of boron, AI-2 exists as R-THMF. (D) Structure of V. cholerae CAI-1 and Amino-CAI-1. (E) Structure of the PQS autoinducer of P. aeruginosa.

A canonical Gram-negative LuxIR-type quorum-sensing system. Red pentagons denote AHL autoinducers. Refer to text for details.

A canonical Gram-positive two-component-type quorum-sensing system. Purple octagons denote processed/modified peptide autoinducers. Refer to text for details.

The V. harveyi quorum-sensing circuit. (A) Signal transduction at LCD. During this stage, autoinducer levels are low and the LuxN, LuxPQ, and CqsS receptors function as kinases. LuxO is phosphorylated, the Qrr1-5 sRNAs are transcribed, and LuxR protein is not produced. (B) Signal transduction at HCD. During this stage, autoinducer levels are high and the LuxN, LuxPQ, and CqsS receptors function as phosphatases. LuxO is unphosphorylated, Qrr1-5 sRNAs are not transcribed, and LuxR protein is produced. Solid and dotted lines denote regulatory factors that are produced and not produced, respectively. Refer to text for details.

The V. harveyi quorum-sensing circuit. (A) Signal transduction at LCD. During this stage, autoinducer levels are low and the LuxN, LuxPQ, and CqsS receptors function as kinases. LuxO is phosphorylated, the Qrr1-5 sRNAs are transcribed, and LuxR protein is not produced. (B) Signal transduction at HCD. During this stage, autoinducer levels are high and the LuxN, LuxPQ, and CqsS receptors function as phosphatases. LuxO is unphosphorylated, Qrr1-5 sRNAs are not transcribed, and LuxR protein is produced. Solid and dotted lines denote regulatory factors that are produced and not produced, respectively. Refer to text for details.

The V. cholerae quorum-sensing circuit. (A) Signal transduction at LCD. During this stage, autoinducer levels are low and the CqsS and LuxPQ receptors function as kinases. LuxO is phosphorylated, the Qrr1-4 sRNAs are transcribed, and HapR protein is not produced. (B) Signal transduction at HCD. During this stage, autoinducer levels are high and the CqsS and LuxPQ receptors function as phosphatases. LuxO is unphosphorylated, Qrr1-4 sRNAs are not transcribed, and HapR protein is produced. Solid and dotted lines denote regulatory factors that are produced and not produced, respectively. Refer to text for details.

The V. cholerae quorum-sensing circuit. (A) Signal transduction at LCD. During this stage, autoinducer levels are low and the CqsS and LuxPQ receptors function as kinases. LuxO is phosphorylated, the Qrr1-4 sRNAs are transcribed, and HapR protein is not produced. (B) Signal transduction at HCD. During this stage, autoinducer levels are high and the CqsS and LuxPQ receptors function as phosphatases. LuxO is unphosphorylated, Qrr1-4 sRNAs are not transcribed, and HapR protein is produced. Solid and dotted lines denote regulatory factors that are produced and not produced, respectively. Refer to text for details.

Reciprocal production of V. harveyi Qrr sRNAs and LuxR leads to temporal control of quorum-sensing target genes. From LCD to HCD, Qrr sRNA levels decrease and LuxR levels increase. As a consequence, Class 3 quorum-sensing target genes, whose promoters have the highest affinity for LuxR, are activated/repressed first, followed by Class 2 genes, and finally Class 1 genes.

Feedback loops identified in the V. harveyi and V. cholerae quorum-sensing networks. Four different feedback loops are integrated into the V. harveyi and V. cholerae quorum-sensing circuits. Arrows denote activation. T-shape arrows denote repression.
Similar articles
-
Mashruwala AA, Bassler BL. Mashruwala AA, et al. mBio. 2020 Jul 28;11(4):e01572-20. doi: 10.1128/mBio.01572-20. mBio. 2020. PMID: 32723922 Free PMC article.
-
Bridges AA, Bassler BL. Bridges AA, et al. PLoS Biol. 2019 Nov 11;17(11):e3000429. doi: 10.1371/journal.pbio.3000429. eCollection 2019 Nov. PLoS Biol. 2019. PMID: 31710602 Free PMC article.
-
Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi.
Henke JM, Bassler BL. Henke JM, et al. J Bacteriol. 2004 Oct;186(20):6902-14. doi: 10.1128/JB.186.20.6902-6914.2004. J Bacteriol. 2004. PMID: 15466044 Free PMC article.
-
Quorum Sensing Gene Regulation by LuxR/HapR Master Regulators in Vibrios.
Ball AS, Chaparian RR, van Kessel JC. Ball AS, et al. J Bacteriol. 2017 Sep 5;199(19):e00105-17. doi: 10.1128/JB.00105-17. Print 2017 Oct 1. J Bacteriol. 2017. PMID: 28484045 Free PMC article. Review.
-
Parallel quorum sensing signaling pathways in Vibrio cholerae.
Jung SA, Hawver LA, Ng WL. Jung SA, et al. Curr Genet. 2016 May;62(2):255-60. doi: 10.1007/s00294-015-0532-8. Epub 2015 Nov 6. Curr Genet. 2016. PMID: 26545759 Free PMC article. Review.
Cited by
-
Kapadia C, Kachhdia R, Singh S, Gandhi K, Poczai P, Alfarraj S, Ansari MJ, Gafur A, Sayyed RZ. Kapadia C, et al. Front Microbiol. 2022 Aug 23;13:977669. doi: 10.3389/fmicb.2022.977669. eCollection 2022. Front Microbiol. 2022. PMID: 36090086 Free PMC article.
-
Microbiome engineering for bioremediation of emerging pollutants.
Singha LP, Shukla P. Singha LP, et al. Bioprocess Biosyst Eng. 2023 Mar;46(3):323-339. doi: 10.1007/s00449-022-02777-x. Epub 2022 Aug 27. Bioprocess Biosyst Eng. 2023. PMID: 36029349 Review.
-
Zhang X, Li Z, Pang S, Jiang B, Yang Y, Duan Q, Zhu G. Zhang X, et al. Arch Microbiol. 2021 Mar;203(2):431-441. doi: 10.1007/s00203-020-02050-3. Epub 2020 Sep 25. Arch Microbiol. 2021. PMID: 32975620 Review.
-
An Evolutionary Fitness Enhancement Conferred by the Circadian System in Cyanobacteria.
Ma P, Woelfle MA, Johnson CH. Ma P, et al. Chaos Solitons Fractals. 2013 May 1;50:65-74. doi: 10.1016/j.chaos.2012.11.006. Chaos Solitons Fractals. 2013. PMID: 23626410 Free PMC article.
-
Frei R, Breitbach AS, Blackwell HE. Frei R, et al. Chem Sci. 2012 May;3(5):1555-1561. doi: 10.1039/C2SC01089E. Chem Sci. 2012. PMID: 23198087 Free PMC article.
References
-
- Austin B, Zhang XH. Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol. 2006;43:119–24. - PubMed
-
- Bassler BL, Wright M, Showalter RE, Silverman MR. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol. 1993;9:773–86. - PubMed
-
- Bassler BL, Wright M, Silverman MR. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol. 1994;13:273–86. - PubMed
-
- Bassler BL, Wright M, Silverman MR. Sequence and function of LuxO, a negative regulator of luminescence in Vibrio harveyi. Mol Microbiol. 1994;12:403–12. - PubMed
Publication types
MeSH terms
Grants and funding
LinkOut - more resources
Full Text Sources
Other Literature Sources