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Chapter 28 : Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence

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Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence, Page 1 of 2

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Abstract:

This chapter focuses on the different molecular mechanisms two model luminous bacteria, (a symbiont) and (a free-living microbe), use for regulating expression. Expression of luminescence in most bacteria is tightly regulated by the density of the population. In , the regulatory genes involved in density-dependent control of luminescence are adjacent to the operon encoding the luciferase enzymes. The regulatory genes that control luminescence in are different from those of . One complementation group of dim mutants could be restored to full light production by a family of recombinant cosmids containing a subset of common restriction fragments. Initial HAI-1 and HAI-2 signal recognition by LuxN and LuxQ could activate a series of phosphotransfer reactions. Two-component circuits have been characterized in which a single protein contains both a sensor kinase and a response regulator domain (similar to LuxN and LuxQ) and a second protein contains both a response regulator domain and a DNA binding motif (similar to LuxO). The differences between the regulatory circuits controlling density-dependent expression of luminescence in and are striking. Subsequent mutations and gene duplications and rearrangements generated new and multiple autoinducers, receptivities, and regulatory connections, finally resulting in a bacterium with the properties of .

Citation: Bassler B, Silverman M. 1995. Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence, p 431-445. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch28

Key Concept Ranking

Signal Transduction
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Signalling Pathway
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Signal Molecules
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Quorum Sensing
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Figures

Image of FIGURE 1
FIGURE 1

Model for regulation of bioluminescence in . Synthesis of the enzymes for light production in is dependent on transcription of operon R, which contains . The product of the gene is not required for luminescence. Transcription of operon R is regulated by the interaction of autoinducer (the production of which is a function of the gene) and the protein LuxR, encoded by the gene. In dilute cell suspensions, weak constitutive transcription of operon R occurs, resulting in a low concentration of autoinducer. As the cell density increases, a concentration of autoinducer is reached that is sufficient to induce transcription of operon R. Because is in operon R, autoinducer synthesis is also increased on induction of operon R. The functions regulating operon R form a positive feedback circuit, and induction of operon R results in an exponential increase in light production per cell. A compensatory negative feedback circuit operates to indirectly modulate the expression of operon R (and light production) after induction. Negative regulation is achieved by limiting the expression of operon L containing and requires the interaction of autoinducer and LuxR. VAI, autoinducer; P and P, left- and rightward promoters, respectively.

Citation: Bassler B, Silverman M. 1995. Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence, p 431-445. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch28
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Image of FIGURE 2
FIGURE 2

Model for genetic control of luminescence in . Expression of the operon () encoding luminescence enzymes is controlled by two signalling channels, signalling systems 1 and 2. Each signalling system consists of functions that produce an extracellular signal substance (Signal 1 or 2) and functions that regulate the response to the corresponding signal substance (Sensor 1 or 2). Each signal substance (autoinducer 1 or 2 denoted by HAI-1 or HAI-2) interacts with the corresponding sensor (O). Signal 1 function is encoded by and , and Sensor 1 function is encoded by . The Sensor 2 function is the product of the and genes, and the gene(s) encoding Signal 2 synthesis function has not been identified. Sensor proteins regulate expression of luminescence indirectly by inactivating LuxO, a repressor of the operon. Expression of also requires LuxR, a positive transcription factor. The interactions and activities of the sensor and repressor proteins are probably controlled by phosphorylation reactions (see text).

Citation: Bassler B, Silverman M. 1995. Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence, p 431-445. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch28
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Image of FIGURE 3
FIGURE 3

Response phenotypes of LuxN and LuxQ transposon insertion mutants of . The wild-type (top panel) is a control strain with a Tn insertion outside the regulatory region. Response curves for transposon insertion mutants with the LuxN (middle panel) and LuxQ (bottom panel) phenotypes are also shown. Bright cultures of these strains were diluted 1:5,000, and light production was then measured during growth of the cultures. Cell-free supernatant (10%) or synthetic autoinducer (1 µg ml) was added at the time of the first measurement. No addition (○), wild-type supernatant (●), LuxM supernatant (i.e., HAI-2 [■]), and synthetic autoinducer (i.e., HAI-1 [□]). Relative light units are denned as light emission per cell (i.e., counts min ml X 10/colony-forming units ml) and are plotted as a function of cell density (colony-forming units/ml). Data were taken from .

Citation: Bassler B, Silverman M. 1995. Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence, p 431-445. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch28
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Image of FIGURE 4
FIGURE 4

Amino acid sequence comparisons between Lux regulatory proteins and members of Arc bacterial two-component sensory transduction system. The protein comparisons were aligned to LuxQ. Amino acid sequence similarities between the histidine protein kinase and response regulator domains of LuxQ, and those domains in LuxN and LuxO and ArcB and ArcA are shown. The symbols “.” and “:” denote amino acid similarities and identities, respectively. The highly conserved H, N, G1, F, and G2 blocks in the histidine protein kinase domain and the Asp-12,13, Asp-57, and Lys-109 blocks in the response regulator domain are boxed in LuxQ. Numbers next to protein designations refer to the position in the protein of the first amino acid residue used in each line of the sequence comparison. The full lengths of the proteins are LuxN, 849; LuxQ, 859; LuxO, 453; ArcB, 778; and ArcA, 238 amino acids.

Citation: Bassler B, Silverman M. 1995. Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence, p 431-445. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch28
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Image of FIGURE 5
FIGURE 5

Two-component signal relay in density-sensing. Density-dependent regulation of luminescence in begins with binding of the signalling system 1 and 2 autoinducers (HAI-1 and HAI-2) by their cognate sensors LuxN and LuxP, Q, respectively. The LuxP protein is similar to the periplasmic ribose binding protein of and . LuxN and LuxQ are members of the bacterial “two-component” family of adaptive response regulators, and each contains a histidine-protein kinase sensor domain and a response regulator domain. Subsequent signal transduction is proposed to occur via a series of phosphorelay reactions (see text). Coupling and integration of the signals from the two pathways could be accomplished by LuxO, a negative regulator of luminescence. LuxO is similar to the response regulator class of two-component regulatory proteins, and it contains a DNA binding domain so it could directly interact with DNA. H, histidine; D, aspartate; and H-T-H, helix-turn-helix DNA binding domain.

Citation: Bassler B, Silverman M. 1995. Intercellular Communication in Marine Species: Density-Dependent Regulation of the Expression of Bioluminescence, p 431-445. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch28
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