Biofilm matrix disrupts nematode motility and predatory behavior

Abstract

In nature, bacteria form biofilms by producing exopolymeric matrix that encases its entire community. While it is widely known that biofilm matrix can prevent bacterivore predation and contain virulence factors for killing predators, it is unclear if they can alter predator motility. Here, we report a novel "quagmire" phenotype, where Pseudomonas aeruginosa biofilms could retard the motility of bacterivorous nematode Caenorhabditis elegans via the production of a specific exopolysaccharide, Psl. Psl could reduce the roaming ability of C. elegans by impeding the slithering velocity of C. elegans. Furthermore, the presence of Psl in biofilms could entrap C. elegans within the matrix, with dire consequences to the nematode. After being trapped in biofilms, C. elegans could neither escape effectively from aversive stimuli (noxious blue light), nor leave easily to graze on susceptible biofilm areas. Hence, this reduced the ability of C. elegans to roam and predate on biofilms. Taken together, our work reveals a new function of motility interference by specific biofilm matrix components, and emphasizes its importance in predator-prey interactions.

Fig. 1. Biofilms impede locomotion and restrict roaming of C. elegans.

a Average velocity, b average displacement, and c representative tracks traveled by C. elegans (N ≥ 150) on OP50, PAO1, ΔwspF, and PAO1/p_lac-YedQ lawns. Means and SD are shown. ***P < 0.001, one-way ANOVA.

Fig. 2. Psl is more important than Pel at impeding nematode locomotion under influence by wsp operon.

a Average velocity, b average displacement, and c representative tracks traveled by C. elegans (N ≥ 150) on EPS mutant lawns. Changes to average distance traveled by C. elegans after exogenous addition of d Pel or e Psl to Pel⁻Psl⁻ strain. Means and SD are shown. **P < 0.01, ***P < 0.001, ns not significant, one-way ANOVA.

Fig. 3. Psl immobilizes and delays C. elegans from escape and attacking susceptible biofilms.

a Schematic representation of trapping C. elegans by biofilms under blue light repulsion. b Duration taken by C. elegans to escape biofilm trap. c Schematic representation of trapping and baiting C. elegans. d Extent of roaming of C. elegans on bait biofilm after leaving the trap biofilm. Means and SD from triplicate experiments are shown. **P < 0.01, ***P < 0.001, ns not significant, one-way ANOVA.

Fig. 4. Role of alginate in the quagmire phenotype.

a Average velocity, b average displacement, and c representative tracks travelled by C. elegans (N ≥ 150) on PAO1, Alg⁺, and Alg⁻ lawns. d Exogenous addition of alginate to Alg⁻ strain. e Duration taken by C. elegans to escape biofilm trap. Means and SD are shown. **P < 0.01, ***P < 0.001, ns not significant, one-way ANOVA.