Bacterial quorum-sensing network architectures

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.

Figure 1

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.

Figure 1

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.

Figure 2

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

Figure 3

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

Figure 4

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.

Figure 4

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.

Figure 5

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.

Figure 5

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.

Figure 6

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.

Figure 7

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.