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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.

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Related in: MedlinePlus

Bioluminescence-growth relationships for the Vh strains that served as wild type references for comparison with mutants in quorum sensing and bioluminescence.The isogenic, wild type Vh strains, (A) BB120, growth rate (□) and RLU or relative light units expressed as counts per second/OD (v) and (B) BB866 (WT::Tn5) in the absence (growth rate (□) and relative light units, (v)) and presence of the antibiotic, kanamycin (growth rate, ⋄ and Relative Light Units, ⧫).
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pone-0001671-g002: Bioluminescence-growth relationships for the Vh strains that served as wild type references for comparison with mutants in quorum sensing and bioluminescence.The isogenic, wild type Vh strains, (A) BB120, growth rate (□) and RLU or relative light units expressed as counts per second/OD (v) and (B) BB866 (WT::Tn5) in the absence (growth rate (□) and relative light units, (v)) and presence of the antibiotic, kanamycin (growth rate, ⋄ and Relative Light Units, ⧫).

Mentions: The growth curves of two isogenic wild type Vh strains are shown in Figure 2. Both strains are wild type with respect to the three known quorum sensing autoinducer receptors (LuxPQ, LuxN, and CqsS) and they respond to all three autoinducers (HAI-1, AI-2, and CAI-1). Strain BB120 is the wild type base strain for these studies. Strain BB866 is V. harveyi BB120, harboring a Tn5 insertion upstream of luxPQ. Strain BB866 was constructed as described in other studies and the inserted transposon has no polar effects on neighboring genes [24]. Strains BB120 and BB866 grew at growth rates of 1.0/H in similarly inoculated wells.


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)

Bioluminescence-growth relationships for the Vh strains that served as wild type references for comparison with mutants in quorum sensing and bioluminescence.The isogenic, wild type Vh strains, (A) BB120, growth rate (□) and RLU or relative light units expressed as counts per second/OD (v) and (B) BB866 (WT::Tn5) in the absence (growth rate (□) and relative light units, (v)) and presence of the antibiotic, kanamycin (growth rate, ⋄ and Relative Light Units, ⧫).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001671-g002: Bioluminescence-growth relationships for the Vh strains that served as wild type references for comparison with mutants in quorum sensing and bioluminescence.The isogenic, wild type Vh strains, (A) BB120, growth rate (□) and RLU or relative light units expressed as counts per second/OD (v) and (B) BB866 (WT::Tn5) in the absence (growth rate (□) and relative light units, (v)) and presence of the antibiotic, kanamycin (growth rate, ⋄ and Relative Light Units, ⧫).
Mentions: The growth curves of two isogenic wild type Vh strains are shown in Figure 2. Both strains are wild type with respect to the three known quorum sensing autoinducer receptors (LuxPQ, LuxN, and CqsS) and they respond to all three autoinducers (HAI-1, AI-2, and CAI-1). Strain BB120 is the wild type base strain for these studies. Strain BB866 is V. harveyi BB120, harboring a Tn5 insertion upstream of luxPQ. Strain BB866 was constructed as described in other studies and the inserted transposon has no polar effects on neighboring genes [24]. Strains BB120 and BB866 grew at growth rates of 1.0/H in similarly inoculated wells.

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