Character displacement and the evolution of niche complementarity in a model biofilm community

Abstract

Colonization of vacant environments may catalyze adaptive diversification and be followed by competition within the nascent community. How these interactions ultimately stabilize and affect productivity are central problems in evolutionary ecology. Diversity can emerge by character displacement, in which selection favors phenotypes that exploit an alternative resource and reduce competition, or by facilitation, in which organisms change the environment and enable different genotypes or species to become established. We previously developed a model of long-term experimental evolution in which bacteria attach to a plastic bead, form a biofilm, and disperse to a new bead. Here, we focus on the evolution of coexisting mutants within a population of Burkholderia cenocepacia and how their interactions affected productivity. Adaptive mutants initially competed for space, but later competition declined, consistent with character displacement and the predicted effects of the evolved mutations. The community reached a stable equilibrium as each ecotype evolved to inhabit distinct, complementary regions of the biofilm. Interactions among ecotypes ultimately became facilitative and enhanced mixed productivity. Observing the succession of genotypes within niches illuminated changing selective forces within the community, including a fundamental role for genotypes producing small colony variants that underpin chronic infections caused by B. cenocepacia.

Evolution of exploitative interactions during diversification in Bacillus subtilis biofilms

“…B. cenocepacia diversified into three distinct morphotypes, the two of which preferentially attached to the polystyrene surface, whereas the third mostly resided on the top of the biofilm (Ellis et al 2015). The productivity of this ecotype mix was elevated due to the so called niche complementarity effect (Poltak and Cooper 2011;Ellis et al 2015). Similar niche specialization was earlier observed in Pseudomonas fluorescens evolved in a static microcosm, where the population .…”

“…Evolutionary diversification tends to improve biofilm productivity as newly emerged variants specialize in occupying different niches thereby reducing competition (Rainey and Travisano 1998;Poltak and Cooper 2011;Ellis et al 2015;Flynn et al 2016). An excellent example derives from a comprehensive study of an opportunistic pathogen, Burkholderia cenocepacia, which was allowed to evolve in a form of submerged biofilm subsequently assembling on a polystyrene bead floating in the liquid medium (Poltak and Cooper 2011).…”

“…An excellent example derives from a comprehensive study of an opportunistic pathogen, Burkholderia cenocepacia, which was allowed to evolve in a form of submerged biofilm subsequently assembling on a polystyrene bead floating in the liquid medium (Poltak and Cooper 2011). B. cenocepacia diversified into three distinct morphotypes, the two of which preferentially attached to the polystyrene surface, whereas the third mostly resided on the top of the biofilm (Ellis et al 2015). The productivity of this ecotype mix was elevated due to the so called niche complementarity effect (Poltak and Cooper 2011;Ellis et al 2015).…”

“…Altogether, experimental studies on adaptation in biofilms seem to share certain scenarios: variants with distinct colony morphology readily emerge; the derived morphotypes differ in biofilm formation capabilities (Rainey and Travisano 1998;Poltak and Cooper 2011;Leiman et al 2014;Flynn et al 2016); these differences result in a new type of spatial arrangement which reduces niche overlap and improves population productivity (Rainey and Travisano 1998;Poltak and Cooper 2011;Ellis et al 2015;Flynn et al 2016;Kim, Levy and Foster 2016). While the evolution in biofilms of medically-relevant Gramnegative microbes (B. cenocepacia and Pseudomonas spp) has been extensively studied, adaptive .…”

Biofilms 2015: Multidisciplinary Approaches Shed Light into Microbial Life on Surfaces

“…By following the evolution of wrinkly colonies from a smooth B. cenocepacia ancestor, a phenomenon associated with biofilm infections, Dr. Cooper showed that selection favored mutations clustered in the wsp operon (43). Despite phenotypic differences among wrinkly mutants, they shared similar fitness properties in mixed biofilms and acted as early surface colonists, suggesting that strong selective forces drive the colonization of this common niche (44). Daniel López (Institute for Molecular Infectious Biology, Würzburg, Germany) described the evolution of antibiotic resistance in Staphylococcus biofilms using intraclonal competition.…”