Complex extracellular biology drives surface competition during colony expansion in Bacillus subtilis

Abstract

Many bacteria grow on surfaces in nature, where they form cell collectives that compete for space. Within these collectives, cells often secrete molecules that benefit surface spreading by, for example, reducing surface tension or promoting filamentous growth. Although we have a detailed understanding of how these molecules are produced, much remains unknown about their role in surface competition. Here we examine sliding motility in Bacillus subtilis and compare how secreted molecules, essential for sliding, affect intraspecific cooperation and competition on a surface. We specifically examine (i) the lipopeptide surfactin, (ii) the hydrophobin protein BslA, and (iii) exopolysaccharides (EPS). We find that these molecules have a distinct effect on surface competition. Whereas surfactin acts like a common good, which is costly to produce and benefits cells throughout the surface, BslA and EPS are cost-free and act locally. Accordingly, surfactin deficient mutants can exploit the wild-type strain in competition for space, while BslA and EPS mutants cannot. Supported by a mathematical model, we show that three factors are important in predicting the outcome of surface competition: the costs of molecule synthesis, the private benefits of molecule production, and the diffusion rate. Our results underscore the intricate extracellular biology that can drive bacterial surface competition.

Breakdown of clonal cooperative architecture in multispecies biofilms and the spatial ecology of predation

“…This study makes explicit that the cellular arrangement and tightly packed structure of clonal V. cholerae groups can operate as a type of public good (39, 91) that confers predator protection to the cells within (among many other benefits (30, 30, 33–35, 55, 74, 92–96)). Other species – here, E. coli , whose mono-species biofilms are susceptible to B. bacteriovorus – can take advantage of this protective architecture when small groups of them become enveloped by expanding, highly packed biofilms of V. cholerae .…”

Signatures of kin selection in a natural population of the bacteriaBacillus subtilis

“…For example, the spatial details of how cooperative interactions play out, such as how far do public goods diffuse, and who benefits, as well as how much these vary in different environments, and the frequency with which different environments are encountered (28, 82). Indeed, cooperative traits in B. subtilis vary in the degree to which they are shared depending on whether groups are exhibiting sliding motility or growing in biofilms (16). In contrast, the indirect measure provided by population genetics represents an average for the different cooperative traits, over the different environments encountered, over evolutionary time.…”

“…We took advantage of the vcf-tools software , which allowed us to randomly remove strains from our analysis. This enabled us to conduct a basic analysis on polymorphism for a groups of N strains (N = 4, 6,8,10,12,14,16,18,20,22,24,26,28), with 22 iterations of each number of strains Within any analysis, we focussed on the 3570 genes which are present in all strains, and calculated mean and median polymorphism (average pairwise polymorphism, relative to gene length) (Supplementary Figure S5.1). S5.1: (A) Median polymorphism, (B) Mean polymorphism as the number of strains uses in the analysis varies.…”

“…The relaxed selection when r < 1 results in an increased probability of fixation for deleterious mutations, and a decreased probability of fixation for beneficial mutations (14)(15)(16). The consequence of this change in fixation probabilities, when r<1, is that it would lead to increased polymorphism and divergence in cooperative genes relative to genes that have direct fitness effects (Figure 1).…”

“…It is hard to know whether the artificial environments and gene knockouts of lab experiments are representative of natural populations. Experiments have also shown that some traits can be cooperative in some environments but private in others (16). Across species comparative studies have shown that cooperation is more common in species where relatedness is higher (17, 18), but this doesn’t help us determine whether specific traits are evolving as cooperative public goods.…”