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EcoSal Plus

Domain 9: Life in Communities and the Environment

Cell-to-Cell Signaling in and

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  • Authors: Melissa M. Kendall1, and Vanessa Sperandio2
  • Editor: David M. Gordon3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology, Immunology, and Cancer Biology, University of Virginia, Charlottesville, VA 22908; 2: Department of Microbiology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390; 3: The Australian National University, Acton
  • Received 03 February 2014 Accepted 24 March 2014 Published 06 June 2014
  • Address correspondence to: Correspondence: Vanessa Sperandio, vanessa.sperandio@utsouthwestern.edu
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  • Abstract:

    Bacteria must be able to respond rapidly to changes in the environment to survive. One means of coordinating gene expression relies on tightly regulated and complex signaling systems. One of the first signaling systems that was described in detail is quorum sensing (QS). During QS, a bacterial cell produces and secretes a signaling molecule called an autoinducer (AI). As the density of the bacterial population increases, so does the concentration of secreted AI molecules, thereby allowing a bacterial species to coordinate gene expression based on population density. Subsequent studies have demonstrated that bacteria are also able to detect signal molecules produced by other species of bacteria as well as hormones produced by their mammalian hosts. This type of signaling interaction has been termed cell-to-cell signaling because it does not rely on a threshold concentration of bacterial cells. This review discusses the three main types of cell-to-cell signaling mechanisms used by and : the LuxR process, in which and detect signals produced by other species of bacteria; the LuxS/AI-2 system, in which and participate in intra- and interspecies signaling; and the AI-3/epinephrine/norepinephrine system, in which and recognize self-produced AI, signal produced by other microbes, and/or the human stress hormones epinephrine and/or norepinephrine.

  • Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013

Key Concept Ranking

Protein Folding
0.4435223
Salmonella enterica
0.41628966
0.4435223

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128. journal-id:
ecosalplus.ESP-0002-2013.citations
ecosalplus/6/1
content/journal/ecosalplus/10.1128/ecosalplus.ESP-0002-2013
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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0002-2013
2014-06-06
2017-05-29

Abstract:

Bacteria must be able to respond rapidly to changes in the environment to survive. One means of coordinating gene expression relies on tightly regulated and complex signaling systems. One of the first signaling systems that was described in detail is quorum sensing (QS). During QS, a bacterial cell produces and secretes a signaling molecule called an autoinducer (AI). As the density of the bacterial population increases, so does the concentration of secreted AI molecules, thereby allowing a bacterial species to coordinate gene expression based on population density. Subsequent studies have demonstrated that bacteria are also able to detect signal molecules produced by other species of bacteria as well as hormones produced by their mammalian hosts. This type of signaling interaction has been termed cell-to-cell signaling because it does not rely on a threshold concentration of bacterial cells. This review discusses the three main types of cell-to-cell signaling mechanisms used by and : the LuxR process, in which and detect signals produced by other species of bacteria; the LuxS/AI-2 system, in which and participate in intra- and interspecies signaling; and the AI-3/epinephrine/norepinephrine system, in which and recognize self-produced AI, signal produced by other microbes, and/or the human stress hormones epinephrine and/or norepinephrine.

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Figures

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Figure 1

LuxI synthesizes AI-1 and diffuses outside the cell. When cell density, and therefore, AI-1 concentration, is high, AI-1 diffuses back into the cell where it binds to LuxR. LuxR complexed with AI-1 subsequently activates transcription of itself as well as the luciferase operon. IM, inner membrane; OM, outer membrane. doi:10.1128/ecosalplus.ESP-0002-2013.f1

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 2

(A) AI-1 is composed of a homoserine lactone ring bound to a fatty acid side chain; (B) SdiA detects oxoC8 and oxoC6 with greatest sensitivities; (C) SdiA can also detect other forms of AI-1 such as C8 and C6, although with less sensitivity. doi:10.1128/ecosalplus.ESP-0002-2013.f2

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 3

Once EHEC enters the rumen, it encounters AHLs. In the presence of AHLs, SdiA is functionally stable and acts to increase expression of acid tolerance genes in the operon and represses expression of the LEE genes. Up-regulation of the genes allows EHEC to survive passage through the acidic abomasum. AHLs have not been detected in the colon; thus, SdiA is unstable, and EHEC can activate the LEE and colonize the RAJ of the colon. doi:10.1128/ecosalplus.ESP-0002-2013.f3

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 4

The and genes carried on this operon affect the transcription and folding, respectively, of plasmid-encoded fimbriae that are encoded by the upstream genes. SrgA plays a role in protein folding in the -encoded fimbriae by catalyzing disulfide bond formation ( 52 , 53 ). ORF, open reading frame. doi:10.1128/ecosalplus.ESP-0002-2013.f4

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 5

In the activated methyl cycle, SAM is converted ultimately to homocysteine and DPD. LuxS catalyzes the last step in the pathway, resulting in DPD. AI-2 is derived from the unstable compound DPD. doi:10.1128/ecosalplus.ESP-0002-2013.f5

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 6

(A) AI-2 produced by is (2,4)-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran-borate (-THMF borate); (B) AI-2 produced by serovar Typhimurium is (2,4)-2-methyl-2,3,3,4-tetrahydroxyte-tetrahydrofuran (-THMF). doi:10.1128/ecosalplus.ESP-0002-2013.f6

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 7

The genes are transcribed in an operon, whereas and are divergently transcribed. LsrB binds AI-2, which is then imported by the Lsr ABC transport system. Inside the cell, AI-2 is phosphorylated by LsrK. Phosphorylated AI-2 interacts with LsrR, and this relieves LsrR-repression of the operon. LsrG depletes the intracellular pool of phosphorylated AI-2, thereby enabling LsrR to re-repress the operon. doi:10.1128/ecosalplus.ESP-0002-2013.f7

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 8

Methionine is important in the cell for production of the vital metabolic enzyme SAM (involved in the methylation of lipids, RNA, DNA, and protein), and de novo synthesis of methionine requires homocysteine. The mutant cannot produce homocysteine through SRH hydrolysis; therefore, the oxaloacetate/-glutamate pathway must be used. Oxaloacetate, -glutamate, and the AspC and TyrB transaminases are used to produce aspartate, which than can proceed through a series of reactions that result in the synthesis of homocysteine. Exclusive use of this pathway may lead to altered metabolism and amino acid content in the mutant, leading to reduced AI-3 synthesis. doi:10.1128/ecosalplus.ESP-0002-2013.f8

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 9

The structure of AI-3 is not known but may resemble the aromatic compounds epinephrine and norepinephrine. doi:10.1128/ecosalplus.ESP-0002-2013.f9

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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Figure 10

AI-3, epinephrine, and norepinephrine bind the membrane receptor protein QseC, resulting in autophosphorylation. Subsequently, QseC phosphorylates its response regulator QseB, initiating a complex phosphorelay signaling cascade that results in expression of the flagellar biosynthesis and motility genes (), Shiga toxin (), the locus of enterocyte effacement (LEE), and a second two-component system, QseEF, that also promotes expression of the LEE. doi:10.1128/ecosalplus.ESP-0002-2013.f10

Citation: Kendall M, Sperandio V. 2014. Cell-to-Cell Signaling in and , EcoSal Plus 2014; doi:10.1128/ecosalplus.ESP-0002-2013
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