Single gene locus changes perturb complex microbial communities as much as apex predator loss

Abstract

Many bacterial species are highly social, adaptively shaping their local environment through the production of secreted molecules. This can, in turn, alter interaction strengths among species and modify community composition. However, the relative importance of such behaviours in determining the structure of complex communities is unknown. Here we show that single-locus changes affecting biofilm formation phenotypes in Bacillus subtilis modify community structure to the same extent as loss of an apex predator and even to a greater extent than loss of B. subtilis itself. These results, from experimentally manipulated multitrophic microcosm assemblages, demonstrate that bacterial social traits are key modulators of the structure of their communities. Moreover, they show that intraspecific genetic variability can be as important as strong trophic interactions in determining community dynamics. Microevolution may therefore be as important as species extinctions in shaping the response of microbial communities to environmental change.

Figure 1. The composition of our experimental microcosms.

(a) Trophic structure. Arrows indicate trophic relationships leading from consumer to prey organisms. (b) Effects of the ΔsinI, ΔsinR and ΔphoA mutations on biofilm formation and colony surface architecture in B. subtilis. Pellicle column depicts top-down images of microtitre wells in which cells have been grown in MSgg medium for 3 days at 22 °C. The colony column shows top-down images of Petri plates containing a 1.5%-Agar MSgg plate that was initially incubated overnight at 37 °C and later kept at room temperature. White scale bar, 4.6mm. Image credits: Dr Aaron J. Bell (Didnium), Yana Eglit (P. aurelia).

Figure 2. Community structure in our experimental treatments.

Normalized (mean-standardized; overall mean represented by dotted line) abundances (mean±s.e.m, n=10) of each of B. subtilis, S. marcescens, Klebsiella, Aeromonas, Colpidium, P. aurelia, P. caudatum and Didinium in each experimental treatment (a–f).

Figure 3. The extent of change in community structure caused by our experimental manipulations.

(a) Non-metric multidimensional scaling ordination showing the variation in community structure among experimental treatments. Only the centroid of each experimental treatment is shown here for clarity. The ordination (stress=0.03) is based on a Euclidian distance matrix calculated from normalized (mean standardized) species abundances. (b) Euclidean distances between the centroid of each treatment and the control treatment (±bootstrapped s.e.m. from 10⁴ samples) and results of associated permutation tests (10⁴ permutations). Didinium and B. subtilis were excluded from these analyses as they are absent from some treatments as part of the experimental design.

Figure 4. Shifts in species abundances along the observed biofilm production gradient in B. subtilis.

Normalized (mean standardized) abundances of each of B. subtilis, S. marcescens, Klebsiella, Aeromonas, Colpidium, P. aurelia, P. caudatum and Didinium along an axis of sociality as regards biofilm production in B. subtilis from low to high.