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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

The influence of inoculation dilution and cell-free culture fluids from Vp cultures on Vp growth rates.Cultures were grown in pre-warmed MB at 37 °C. Representative graphs: (A) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are: (▪) 1∶10, (•) 1∶102, (▴) 1∶103, (♦) 1∶104, (▾) 1∶105 and (Open Square with Diagonal Line Running from Upper right corner to Lower left corner) 1∶106. (B) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are the same as in panel A. The table shows the corresponding growth rates for each of the dilutions.
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pone-0001671-g005: The influence of inoculation dilution and cell-free culture fluids from Vp cultures on Vp growth rates.Cultures were grown in pre-warmed MB at 37 °C. Representative graphs: (A) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are: (▪) 1∶10, (•) 1∶102, (▴) 1∶103, (♦) 1∶104, (▾) 1∶105 and (Open Square with Diagonal Line Running from Upper right corner to Lower left corner) 1∶106. (B) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are the same as in panel A. The table shows the corresponding growth rates for each of the dilutions.

Mentions: A candidate for a rapidly growing isolate of the marine bacterium Vp was the kind gift of Rita Colwell (UM4552; see strain table 1). The rapid growth rate was confirmed with manual readings from flask cultures maintained at 37°C and conventional spectrophotometry and flow cytometry (data not shown) as well as the microtiter plate method for which readings were taken every 2.5 minutes. UM4552, like other reported Vp isolates, contained all the Vh-like quorum genes as judged by PCR (Table S1). In addition, its growth rate increased about 1.7-fold when an exponential UM4552 culture was diluted up to 1∶106 (see Figure 5 and Table 4) .


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 influence of inoculation dilution and cell-free culture fluids from Vp cultures on Vp growth rates.Cultures were grown in pre-warmed MB at 37 °C. Representative graphs: (A) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are: (▪) 1∶10, (•) 1∶102, (▴) 1∶103, (♦) 1∶104, (▾) 1∶105 and (Open Square with Diagonal Line Running from Upper right corner to Lower left corner) 1∶106. (B) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are the same as in panel A. The table shows the corresponding growth rates for each of the dilutions.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001671-g005: The influence of inoculation dilution and cell-free culture fluids from Vp cultures on Vp growth rates.Cultures were grown in pre-warmed MB at 37 °C. Representative graphs: (A) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are: (▪) 1∶10, (•) 1∶102, (▴) 1∶103, (♦) 1∶104, (▾) 1∶105 and (Open Square with Diagonal Line Running from Upper right corner to Lower left corner) 1∶106. (B) UM4552 culture was diluted and growth curves are starting at different cell densities. The dilutions are the same as in panel A. The table shows the corresponding growth rates for each of the dilutions.
Mentions: A candidate for a rapidly growing isolate of the marine bacterium Vp was the kind gift of Rita Colwell (UM4552; see strain table 1). The rapid growth rate was confirmed with manual readings from flask cultures maintained at 37°C and conventional spectrophotometry and flow cytometry (data not shown) as well as the microtiter plate method for which readings were taken every 2.5 minutes. UM4552, like other reported Vp isolates, contained all the Vh-like quorum genes as judged by PCR (Table S1). In addition, its growth rate increased about 1.7-fold when an exponential UM4552 culture was diluted up to 1∶106 (see Figure 5 and Table 4) .

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