Limits...
Quorum sensing influences Vibrio harveyi growth rates in a manner not fully accounted for by the marker effect of bioluminescence.

Nackerdien ZE, Keynan A, Bassler BL, Lederberg J, Thaler DS - PLoS ONE (2008)

Bottom Line: Vh quorum sensing mutants showed altered growth rates that do not always rank with their relative increase or decrease in bioluminescence.In addition, the cell-free culture fluids of a rapidly growing Vibrio parahaemolyticus (Vp) strain increased the growth rate of wild type Vh without significantly altering Vh's bioluminescence.The effect of quorum sensing on Vh growth rate can be either positive or negative and includes both bioluminescence-dependent and independent components.

View Article: PubMed Central - PubMed

Affiliation: Raymond and Beverly Sackler Laboratory of Molecular Genetics and Informatics, Rockefeller University, New York, New York, USA.

ABSTRACT

Background: The light-emitting Vibrios provide excellent material for studying the interaction of cellular communication with growth rate because bioluminescence is a convenient marker for quorum sensing. However, the use of bioluminescence as a marker is complicated because bioluminescence itself may affect growth rate, e.g. by diverting energy.

Methodology/principal findings: The marker effect was explored via growth rate studies in isogenic Vibrio harveyi (Vh) strains altered in quorum sensing on the one hand, and bioluminescence on the other. By hypothesis, growth rate is energy limited: mutants deficient in quorum sensing grow faster because wild type quorum sensing unleashes bioluminescence and bioluminescence diverts energy. Findings reported here confirm a role for bioluminescence in limiting Vh growth rate, at least under the conditions tested. However, the results argue that the bioluminescence is insufficient to explain the relationship of growth rate and quorum sensing in Vh. A Vh mutant for all genes encoding the bioluminescence pathway grew faster than wild type but not as fast as mutants in quorum sensing. Vh quorum sensing mutants showed altered growth rates that do not always rank with their relative increase or decrease in bioluminescence. In addition, the cell-free culture fluids of a rapidly growing Vibrio parahaemolyticus (Vp) strain increased the growth rate of wild type Vh without significantly altering Vh's bioluminescence. The same cell-free culture fluid increased the bioluminescence of Vh quorum mutants.

Conclusions/significance: The effect of quorum sensing on Vh growth rate can be either positive or negative and includes both bioluminescence-dependent and independent components. Bioluminescence tends to slow growth rate but not enough to account for the effects of quorum sensing on growth rate.

Show MeSH

Related in: MedlinePlus

The overall structure of the Vh quorum sensing circuit showing quorum genes mutated in this work.Vh has three quorum sensing systems that regulate the genes specifying biofilm formation, a type III secretion system, a secreted metalloprotease, bioluminescence (luxCDABE) and other quorum sensing activated- and repressed-genes. System 1 is composed of an autoinducer, HAI-1 (triangles) and its cognate sensor, LuxN. System 2 is composed of autoinducer-2 (pentagons) and the sensor, LuxPQ. System 3 is composed of an intragenera signal, CAI-1 and its cognate sensor, CqsS. At low cell densities, autoinducer signals and phosphate (P) flow act in a negative manner to repress autoinducer genes, and at high cell densities the phosphate flow is reversed and signals act in a positive manner to activate some of the quorum-dependent genes e.g. luciferase. See Introduction for further details. OM, outer membrane; IM, inner membrane.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2249925&req=5

pone-0001671-g001: The overall structure of the Vh quorum sensing circuit showing quorum genes mutated in this work.Vh has three quorum sensing systems that regulate the genes specifying biofilm formation, a type III secretion system, a secreted metalloprotease, bioluminescence (luxCDABE) and other quorum sensing activated- and repressed-genes. System 1 is composed of an autoinducer, HAI-1 (triangles) and its cognate sensor, LuxN. System 2 is composed of autoinducer-2 (pentagons) and the sensor, LuxPQ. System 3 is composed of an intragenera signal, CAI-1 and its cognate sensor, CqsS. At low cell densities, autoinducer signals and phosphate (P) flow act in a negative manner to repress autoinducer genes, and at high cell densities the phosphate flow is reversed and signals act in a positive manner to activate some of the quorum-dependent genes e.g. luciferase. See Introduction for further details. OM, outer membrane; IM, inner membrane.

Mentions: Growth rate and bioluminescence experiments were carried out on an isogenic set of Vibrio harveyi mutants. The three autoinducer-sensor systems comprising the Vh system are described in Figure 1: Autoinducer-1 (denoted HAI-1 for V. harveyi autoinducer-1; N- (3′-hydroxybutanoyl) homoserine lactone), Autoinducer-2 (AI-2, a furanosyl borate diester) and the third autoinducer called CAI-1 (for Cholerae Autoinducer-1;(S)-3-hydroxytridecan-4-one [21]) have been studied in detail in Vibrio harveyi (see Figure 1), where they are involved in the regulation of bioluminescence and dozens of other traits. HAI-1 is produced by LuxM and is detected by LuxN. LuxM and HAI-1 activity appears to be restricted to Vh and the closely related species Vibrio parahaemolyticus (Vp), indicating that this signal is relatively species-specific. Two proteins, LuxP and LuxQ, function together to detect AI-2 (unborated precursor synthesized by LuxS). LuxS and AI-2 production are widespread in the bacterial world, and AI-2 is proposed to be an inter-species communication signal. CAI-1 is made by CqsA and interacts with its cognate sensor, CqsS. The CAI-1-CqsS system is found predominantly in Vibrios, suggesting it could be a genus-specific system. CAI-1 differs from HAI-1 and AI-2 by being detected at extremely low cell densities [22]. The cell-density-dependent information supplied by all three signals is channeled into the cytoplasm by a phosphorylation cascade that converges on a protein called LuxO [23]. LuxO negatively regulates the expression of luxR, encoding the master transcription factor, by activating the expression of multiple small RNAs (sRNAs) that together with the chaperone Hfq, destabilize the luxR mRNA. At high cell densities, LuxO is inactive and so it cannot promote expression of the genes encoding the sRNAs, the luxR mRNA is stabilized, LuxR is produced, and it initiates quorum sensing-controlled behaviors such as expression of the luciferase operon (luxCDABEGH). The luciferase enzyme is composed of two proteins, LuxA and LuxB, while additional proteins, LuxC, LuxD and LuxE are responsible for recycling the aldehyde substrate (for a comprehensive review, see [13]).


Quorum sensing influences Vibrio harveyi growth rates in a manner not fully accounted for by the marker effect of bioluminescence.

Nackerdien ZE, Keynan A, Bassler BL, Lederberg J, Thaler DS - PLoS ONE (2008)

The overall structure of the Vh quorum sensing circuit showing quorum genes mutated in this work.Vh has three quorum sensing systems that regulate the genes specifying biofilm formation, a type III secretion system, a secreted metalloprotease, bioluminescence (luxCDABE) and other quorum sensing activated- and repressed-genes. System 1 is composed of an autoinducer, HAI-1 (triangles) and its cognate sensor, LuxN. System 2 is composed of autoinducer-2 (pentagons) and the sensor, LuxPQ. System 3 is composed of an intragenera signal, CAI-1 and its cognate sensor, CqsS. At low cell densities, autoinducer signals and phosphate (P) flow act in a negative manner to repress autoinducer genes, and at high cell densities the phosphate flow is reversed and signals act in a positive manner to activate some of the quorum-dependent genes e.g. luciferase. See Introduction for further details. OM, outer membrane; IM, inner membrane.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2249925&req=5

pone-0001671-g001: The overall structure of the Vh quorum sensing circuit showing quorum genes mutated in this work.Vh has three quorum sensing systems that regulate the genes specifying biofilm formation, a type III secretion system, a secreted metalloprotease, bioluminescence (luxCDABE) and other quorum sensing activated- and repressed-genes. System 1 is composed of an autoinducer, HAI-1 (triangles) and its cognate sensor, LuxN. System 2 is composed of autoinducer-2 (pentagons) and the sensor, LuxPQ. System 3 is composed of an intragenera signal, CAI-1 and its cognate sensor, CqsS. At low cell densities, autoinducer signals and phosphate (P) flow act in a negative manner to repress autoinducer genes, and at high cell densities the phosphate flow is reversed and signals act in a positive manner to activate some of the quorum-dependent genes e.g. luciferase. See Introduction for further details. OM, outer membrane; IM, inner membrane.
Mentions: Growth rate and bioluminescence experiments were carried out on an isogenic set of Vibrio harveyi mutants. The three autoinducer-sensor systems comprising the Vh system are described in Figure 1: Autoinducer-1 (denoted HAI-1 for V. harveyi autoinducer-1; N- (3′-hydroxybutanoyl) homoserine lactone), Autoinducer-2 (AI-2, a furanosyl borate diester) and the third autoinducer called CAI-1 (for Cholerae Autoinducer-1;(S)-3-hydroxytridecan-4-one [21]) have been studied in detail in Vibrio harveyi (see Figure 1), where they are involved in the regulation of bioluminescence and dozens of other traits. HAI-1 is produced by LuxM and is detected by LuxN. LuxM and HAI-1 activity appears to be restricted to Vh and the closely related species Vibrio parahaemolyticus (Vp), indicating that this signal is relatively species-specific. Two proteins, LuxP and LuxQ, function together to detect AI-2 (unborated precursor synthesized by LuxS). LuxS and AI-2 production are widespread in the bacterial world, and AI-2 is proposed to be an inter-species communication signal. CAI-1 is made by CqsA and interacts with its cognate sensor, CqsS. The CAI-1-CqsS system is found predominantly in Vibrios, suggesting it could be a genus-specific system. CAI-1 differs from HAI-1 and AI-2 by being detected at extremely low cell densities [22]. The cell-density-dependent information supplied by all three signals is channeled into the cytoplasm by a phosphorylation cascade that converges on a protein called LuxO [23]. LuxO negatively regulates the expression of luxR, encoding the master transcription factor, by activating the expression of multiple small RNAs (sRNAs) that together with the chaperone Hfq, destabilize the luxR mRNA. At high cell densities, LuxO is inactive and so it cannot promote expression of the genes encoding the sRNAs, the luxR mRNA is stabilized, LuxR is produced, and it initiates quorum sensing-controlled behaviors such as expression of the luciferase operon (luxCDABEGH). The luciferase enzyme is composed of two proteins, LuxA and LuxB, while additional proteins, LuxC, LuxD and LuxE are responsible for recycling the aldehyde substrate (for a comprehensive review, see [13]).

Bottom Line: Vh quorum sensing mutants showed altered growth rates that do not always rank with their relative increase or decrease in bioluminescence.In addition, the cell-free culture fluids of a rapidly growing Vibrio parahaemolyticus (Vp) strain increased the growth rate of wild type Vh without significantly altering Vh's bioluminescence.The effect of quorum sensing on Vh growth rate can be either positive or negative and includes both bioluminescence-dependent and independent components.

View Article: PubMed Central - PubMed

Affiliation: Raymond and Beverly Sackler Laboratory of Molecular Genetics and Informatics, Rockefeller University, New York, New York, USA.

ABSTRACT

Background: The light-emitting Vibrios provide excellent material for studying the interaction of cellular communication with growth rate because bioluminescence is a convenient marker for quorum sensing. However, the use of bioluminescence as a marker is complicated because bioluminescence itself may affect growth rate, e.g. by diverting energy.

Methodology/principal findings: The marker effect was explored via growth rate studies in isogenic Vibrio harveyi (Vh) strains altered in quorum sensing on the one hand, and bioluminescence on the other. By hypothesis, growth rate is energy limited: mutants deficient in quorum sensing grow faster because wild type quorum sensing unleashes bioluminescence and bioluminescence diverts energy. Findings reported here confirm a role for bioluminescence in limiting Vh growth rate, at least under the conditions tested. However, the results argue that the bioluminescence is insufficient to explain the relationship of growth rate and quorum sensing in Vh. A Vh mutant for all genes encoding the bioluminescence pathway grew faster than wild type but not as fast as mutants in quorum sensing. Vh quorum sensing mutants showed altered growth rates that do not always rank with their relative increase or decrease in bioluminescence. In addition, the cell-free culture fluids of a rapidly growing Vibrio parahaemolyticus (Vp) strain increased the growth rate of wild type Vh without significantly altering Vh's bioluminescence. The same cell-free culture fluid increased the bioluminescence of Vh quorum mutants.

Conclusions/significance: The effect of quorum sensing on Vh growth rate can be either positive or negative and includes both bioluminescence-dependent and independent components. Bioluminescence tends to slow growth rate but not enough to account for the effects of quorum sensing on growth rate.

Show MeSH
Related in: MedlinePlus