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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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(A) Cell-free culture fluid from Vibrio parahaemolyticus influenced the growth rates of Vibrio harveyi.In these experiments, Vh BB120 served as the wild-type reference strain. BB120, WT in MB (○); BB120, WT in 10% Vp UM4552 cell-free culture fluids (•) (B) Vh bioluminescence phenotypes in the absence (white bars) and presence (gray bars) of Vp cell-free culture fluids. Strain designations are: BB120 (WT); BB170 (luxN); BB886 (luxPQ); JMH598 (cqsS) and JMH628 (luxN, luxPQ, cqsS). The accompanying table shows growth rates for each Vh strain in the absence and presence of 10% Vp (UM4552) cell-free culture fluids.
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pone-0001671-g006: (A) Cell-free culture fluid from Vibrio parahaemolyticus influenced the growth rates of Vibrio harveyi.In these experiments, Vh BB120 served as the wild-type reference strain. BB120, WT in MB (○); BB120, WT in 10% Vp UM4552 cell-free culture fluids (•) (B) Vh bioluminescence phenotypes in the absence (white bars) and presence (gray bars) of Vp cell-free culture fluids. Strain designations are: BB120 (WT); BB170 (luxN); BB886 (luxPQ); JMH598 (cqsS) and JMH628 (luxN, luxPQ, cqsS). The accompanying table shows growth rates for each Vh strain in the absence and presence of 10% Vp (UM4552) cell-free culture fluids.

Mentions: Vp and Vh are related and may occupy related [28], though probably not identical [29], ecological niches. The influence of UM4552 cell-free culture fluids on Vh was assayed. 10% Cell free culture-fluid from a fresh saturated culture of UM4552 was added to cultures inoculated with wild type Vh and quorum sensor mutants. Wild type Vibrio harveyi responded differently to Vp cell-free culture fluids than did the quorum mutants. The addition of the cell-free culture fluids led to a prolonged lag phase followed by a significantly faster growth rate of 1.5/H in the wild type Vh compared to a growth rate of 1/H for the wild type Vh in MB alone (Figure 6A). Although growth rate of the mutants was less affected than wild type, the peak luminescence for two of the mutants was increased in the presence of Vp cell-free culture fluids whereas wild type luminescence was not increased (Table 5; Figure 6B). Specifically, the addition of the Vp UM4552 cell-free culture fluids increased light production ca 50 fold in Vh strains possessing LuxPQ and CqsS (BB170) or LuxN and CqsS (BB886). However, only modest increases in light production occurred following addition of UM4552 fluids to mutants lacking the CAI-1 receptor CqsS (JMH598 and JMH628) (Figure 6B).


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)

(A) Cell-free culture fluid from Vibrio parahaemolyticus influenced the growth rates of Vibrio harveyi.In these experiments, Vh BB120 served as the wild-type reference strain. BB120, WT in MB (○); BB120, WT in 10% Vp UM4552 cell-free culture fluids (•) (B) Vh bioluminescence phenotypes in the absence (white bars) and presence (gray bars) of Vp cell-free culture fluids. Strain designations are: BB120 (WT); BB170 (luxN); BB886 (luxPQ); JMH598 (cqsS) and JMH628 (luxN, luxPQ, cqsS). The accompanying table shows growth rates for each Vh strain in the absence and presence of 10% Vp (UM4552) cell-free culture fluids.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001671-g006: (A) Cell-free culture fluid from Vibrio parahaemolyticus influenced the growth rates of Vibrio harveyi.In these experiments, Vh BB120 served as the wild-type reference strain. BB120, WT in MB (○); BB120, WT in 10% Vp UM4552 cell-free culture fluids (•) (B) Vh bioluminescence phenotypes in the absence (white bars) and presence (gray bars) of Vp cell-free culture fluids. Strain designations are: BB120 (WT); BB170 (luxN); BB886 (luxPQ); JMH598 (cqsS) and JMH628 (luxN, luxPQ, cqsS). The accompanying table shows growth rates for each Vh strain in the absence and presence of 10% Vp (UM4552) cell-free culture fluids.
Mentions: Vp and Vh are related and may occupy related [28], though probably not identical [29], ecological niches. The influence of UM4552 cell-free culture fluids on Vh was assayed. 10% Cell free culture-fluid from a fresh saturated culture of UM4552 was added to cultures inoculated with wild type Vh and quorum sensor mutants. Wild type Vibrio harveyi responded differently to Vp cell-free culture fluids than did the quorum mutants. The addition of the cell-free culture fluids led to a prolonged lag phase followed by a significantly faster growth rate of 1.5/H in the wild type Vh compared to a growth rate of 1/H for the wild type Vh in MB alone (Figure 6A). Although growth rate of the mutants was less affected than wild type, the peak luminescence for two of the mutants was increased in the presence of Vp cell-free culture fluids whereas wild type luminescence was not increased (Table 5; Figure 6B). Specifically, the addition of the Vp UM4552 cell-free culture fluids increased light production ca 50 fold in Vh strains possessing LuxPQ and CqsS (BB170) or LuxN and CqsS (BB886). However, only modest increases in light production occurred following addition of UM4552 fluids to mutants lacking the CAI-1 receptor CqsS (JMH598 and JMH628) (Figure 6B).

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