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Chapter 20 : Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits
Authors:
Brian Hammer1,
Bonnie L. Bassler2
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Affiliations:
1: Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544-1014;
2: Howard Hughes Medical Institute, Chevy Chase, MD 20815;
3: Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544-1014
Content Type: Monograph
Publication Year:
2008
Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis
Book DOI:
10.1128/9781555815578
Chapter DOI:
10.1128/9781555815578.ch20
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Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits, Page 1 of 2
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Abstract:
The marine animal pathogen Vibrio harveyi and the human pathogen Vibrio cholerae are aquatic bacteria that engage in a process of cell-cell communication called quorum sensing (QS). Autoinducer (AI)-2 is derived from S-adenosylmethionine in three enzymatic steps. First, S-adenosylmethionine serves as a methyl donor for many biochemical processes, and these methyltransferase-dependent reactions yield S-adenosylhomocysteine. Second, S-adenosylhomocysteine is metabolized to adenine and S-ribosylhomocysteine by the enzyme Pfs, and third, S-ribosylhomocysteine is the substrate for the LuxS enzyme. In mixed species consortia, other microbes also have the potential to alter AI-2 levels, and other classes of AIs are clearly manipulated, but the authors have restricted the discussion to AI-2 and how that pertains to Vibrio QS. Appropriate and distinct responses to potentially different communities are possible because of signal integration in the Vibrio circuits. Channel proteins LsrC and LsrD mediate the delivery of the ligand across the membrane. LsrA is an ATPase that supplies the energy required for transport. Rapid Lsr-dependent transport of R-THMF into the cell occurs at high cell densities. Recent studies in V. harveyi show that it possesses five qrr genes, like its closest Vibrio relatives. Examination of their functions reveals that, in stark contrast to V. cholerae, in V. harveyi the quorum-regulatory RNAs (Qrr) sRNAs act additively to control luxR mRNA levels.
Citation:
Hammer B, Bassler B.
2008.
Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits,
p 323-332.
In
Winans S, Bassler B (ed),
Chemical Communication among Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815578.ch20
Figures
Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits
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Citation:
Hammer B, Bassler B.
2008.
Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits,
p 323-332.
In
Winans S, Bassler B (ed),
Chemical Communication among Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815578.ch20
/content/10.1128/9781555815578.ch20.ch20fig01
FIGURE 1
Model of the V. harveyi quorum-sensing system. Three parallel sensory systems converge to regulate quorum-sensing gene expression by controlling the activity of LuxO. The three autoinducers are CAI-1 (circles), HAI-1 (pentagons), and AI-2 (triangles). LuxO~P, along with σ54, activates transcription of the genes encoding the Qrr sRNAs that indirectly regulate LuxR protein levels by destabilizing the luxR mRNA. This process is mediated by the sRNA chaperone Hfq. Alterations in the transcription of the multiple sRNAs, in turn, produce an increasing gradient of LuxR protein as the cells transition from low to high cell density. Question marks denote additional regulators proposed to control qrr expression. OM, outer membrane;IM, inner membrane.
10.1128/9781555815578/f0324-01_thmb.gif
10.1128/9781555815578/f0324-01.gif
FIGURE 1
Model of the V. harveyi quorum-sensing system. Three parallel sensory systems converge to regulate quorum-sensing gene expression by controlling the activity of LuxO. The three autoinducers are CAI-1 (circles), HAI-1 (pentagons), and AI-2 (triangles). LuxO~P, along with σ54, activates transcription of the genes encoding the Qrr sRNAs that indirectly regulate LuxR protein levels by destabilizing the luxR mRNA. This process is mediated by the sRNA chaperone Hfq. Alterations in the transcription of the multiple sRNAs, in turn, produce an increasing gradient of LuxR protein as the cells transition from low to high cell density. Question marks denote additional regulators proposed to control qrr expression. OM, outer membrane;IM, inner membrane.
Citation:
Hammer B, Bassler B.
2008.
Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits,
p 323-332.
In
Winans S, Bassler B (ed),
Chemical Communication among Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815578.ch20
/content/10.1128/9781555815578.ch20.ch20fig02
FIGURE 2
Model of the V. cholerae quorum-sensing system. Multiple sensory systems converge to regulate quorum-sensing gene expression by controlling the activity and/or levels of LuxO. The two autoinducers are CAI-1 (circles) and AI-2 (triangles). (A) Low cell density: The two quorumsensing circuits (CAI- 1/CqsS and AI-2/LuxPQ) and the VarS/VarA-CsrA/BCD global regulatory system function in conjunction with Fis to increase the amount and/or activity of LuxO-phosphate. LuxO~P, along with σ54, activates transcription of the genes encoding the Qrr sRNAs. The Qrr sRNAs indirectly regulate HapR protein levels by destabilizing the hapR mRNA. This process is mediated by the RNA chaperone Hfq. (B) High cell density: Phosphate is drained from LuxO. Fis and VarS/A-CsrA/BCD are inactive. Under these conditions, hapR mRNA is stabilized and HapR protein is produced. The lightning bolt represents the putative signal detected by VarS. Dotted lines denote hypothetical interactions. OM, outer membrane;IM, inner membrane.
10.1128/9781555815578/f0326-01_thmb.gif
10.1128/9781555815578/f0326-01.gif
FIGURE 2
Model of the V. cholerae quorum-sensing system. Multiple sensory systems converge to regulate quorum-sensing gene expression by controlling the activity and/or levels of LuxO. The two autoinducers are CAI-1 (circles) and AI-2 (triangles). (A) Low cell density: The two quorumsensing circuits (CAI- 1/CqsS and AI-2/LuxPQ) and the VarS/VarA-CsrA/BCD global regulatory system function in conjunction with Fis to increase the amount and/or activity of LuxO-phosphate. LuxO~P, along with σ54, activates transcription of the genes encoding the Qrr sRNAs. The Qrr sRNAs indirectly regulate HapR protein levels by destabilizing the hapR mRNA. This process is mediated by the RNA chaperone Hfq. (B) High cell density: Phosphate is drained from LuxO. Fis and VarS/A-CsrA/BCD are inactive. Under these conditions, hapR mRNA is stabilized and HapR protein is produced. The lightning bolt represents the putative signal detected by VarS. Dotted lines denote hypothetical interactions. OM, outer membrane;IM, inner membrane.
Citation:
Hammer B, Bassler B.
2008.
Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits,
p 323-332.
In
Winans S, Bassler B (ed),
Chemical Communication among Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815578.ch20
/content/10.1128/9781555815578.ch20.ch20fig03
FIGURE 3
Chemistry of AI-2 signaling molecules. Model showing the proposed pathways for the formation of AI-2 signaling molecules recognized by V. harveyi (upper branch) and enteric bacteria (lower branch). Both signals are derived from the common precursor DPD, the product of the LuxS reaction. S-THMF-borate binds to the V. harveyi receptor LuxP, whereas R-THMF binds to the enteric receptor LsrB. Adapted from reference
32
with permission from Elsevier.
10.1128/9781555815578/f0328-01_thmb.gif
10.1128/9781555815578/f0328-01.gif
FIGURE 3
Chemistry of AI-2 signaling molecules. Model showing the proposed pathways for the formation of AI-2 signaling molecules recognized by V. harveyi (upper branch) and enteric bacteria (lower branch). Both signals are derived from the common precursor DPD, the product of the LuxS reaction. S-THMF-borate binds to the V. harveyi receptor LuxP, whereas R-THMF binds to the enteric receptor LsrB. Adapted from reference 32 with permission from Elsevier.
Citation:
Hammer B, Bassler B.
2008.
Signal Integration in the Vibrio harveyi and Vibrio cholerae Quorum-Sensing Circuits,
p 323-332.
In
Winans S, Bassler B (ed),
Chemical Communication among Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815578.ch20
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