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. 2011 Aug 23;108(34):14181-5.
doi: 10.1073/pnas.1111147108. Epub 2011 Aug 8.

A Fitness Trade-Off Between Local Competition and Dispersal in Vibrio Cholerae Biofilms

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Free PMC article

A Fitness Trade-Off Between Local Competition and Dispersal in Vibrio Cholerae Biofilms

Carey D Nadell et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Bacteria commonly grow in densely populated surface-bound communities, termed biofilms, where they gain benefits including superior access to nutrients and resistance to environmental insults. The secretion of extracellular polymeric substances (EPS), which bind bacterial collectives together, is ubiquitously associated with biofilm formation. It is generally assumed that EPS secretion is a cooperative phenotype that benefits all neighboring cells, but in fact little is known about the competitive and evolutionary dynamics of EPS production. By studying Vibrio cholerae biofilms in microfluidic devices, we show that EPS-producing cells selectively benefit their clonemates and gain a dramatic advantage in competition against an isogenic EPS-deficient strain. However, this advantage carries an ecological cost beyond the energetic requirement for EPS production: EPS-producing cells are impaired for dispersal to new locations. Our study establishes that a fundamental tradeoff between local competition and dispersal exists among bacteria. Furthermore, this tradeoff can be governed by a single phenotype.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Competition between EPS-producing (EPS+) and nonproducing (EPS) V. cholerae strains in biofilms and in well-mixed liquid environments. (A) Left: When growing in biofilm monocultures, the EPS+ strain (white bar) accumulates more biovolume per unit area of substratum than does the EPS strain (black bar). Right: The EPS+ strain is unaffected by coinoculation with the EPS strain (white bar), whereas the EPS strain's accumulated biovolume decreases by 80% when grown in coculture with EPS+ cells (black bar). Error bars denote SEM (n = 5). (B) Final frequency of the EPS+ strain is plotted against its initial frequency. In biofilms (closed circles), the EPS+ strain increases in frequency. In shaken liquid environments (open circles), the EPS+ strain decreases in frequency in accordance with model predictions (black line) based on its lower maximum growth rate relative to the EPS strain. Error bars denote SD (biofilm experiments, n = 10–16; liquid experiments, n = 3).
Fig. 2.
Fig. 2.
A time-series of EPS+ cells (red) growing in a biofilm with EPS cells (blue). The initial frequency of EPS+ cells is <5%, and its final frequency is >90%. At 36 h the upper surfaces of some EPS+ cell clusters appear flat because they have reached the ceiling of the chamber in which they are growing. Grid boxes are 11 μm on a side.
Fig. 3.
Fig. 3.
A time-series showing the frequency of EPS+ cells in the biofilm and effluent phases of microfluidic flow chambers, when growing in competition with EPS cells. The EPS+ strain rapidly increases in frequency relative to the EPS strain within the biofilm (closed circles). In the effluent phase of the culture, EPS+ cells do increase in frequency over time (open circles), but more slowly than they do within the biofilm. Error bars denote SD (n = 4).
Fig. 4.
Fig. 4.
Competition between EPS+ and EPS cells within biofilms and for access to new resource patches. (A) The frequency of the EPS+ strain within biofilms is plotted as a function of time. Error bars denote SD (n = 3). (B) Weak disturbance: effluent from chambers containing growing biofilms was diverted to new chambers at 20 h and 46 h. The biovolumes of EPS+ cells (white bars) and EPS cells (black bars) in the newly formed monolayers are shown for both time points. (C) Severe disturbance: flow velocity through biofilm chambers was increased 1,000-fold at 20 and 46 h in separate replicates, and the effluent was used to colonize new chambers as in B.

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