Ecological succession in long-term experimentally evolved biofilms produces synergistic communities

Abstract

Many biofilm populations are known for their exceptional biodiversity, but the relative contributions of the forces that could produce this diversity are poorly understood. This uncertainty grows in the old, well-established communities found on many natural surfaces and in long-term, chronic infections. If the prevailing interactions among species within biofilms are positive, productivity should increase with diversity, but if they tend towards competition or antagonism, productivity should decrease. Here, we describe the parallel evolution of synergistic communities derived from a clone of Burkholderia cenocepacia during B1500 generations of biofilm selection. This long-term evolution was enabled by a new experimental method that selects for daily cycles of colonization, biofilm assembly and dispersal. Each of the six replicate biofilm populations underwent a common pattern of adaptive morphological diversification, in which three ecologically distinct morphotypes arose in the same order of succession and persisted. In two focal populations, mixed communities were more productive than any monoculture and each variant benefited from the mixture. These gains in output resulted from asymmetrical cross-feeding between ecotypes and the expansion and partitioning of biofilm space that constructed new niches. Therefore, even in the absence of starting genetic variation, prolonged selection for surface colonization generates a dynamic of ecological succession that enhances productivity.

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 .…”

“…Due to large population sizes coupled with short generation times, bacterial adaptation can be observed in a course of days or months, allowing for its experimental investigation (Kawecki et al 2012;Rosenzweig and Sherlock 2014;Martin et al 2016). Experimental evolution studies continuously deepen our understanding of microbial adaptation, revealing common evolutionary scenarios such as genome reduction (Nilsson et al 2005) or genome rearrangements (Martin et al 2017), hypermutability (Flynn et al 2016;Tenaillon et al 2016), or diversification (Rainey and Travisano 1998;Poltak and Cooper 2011;Koch et al 2014;Flynn et al 2016;Kim, Levy and Foster 2016). The last one, where microbes diversify into distinct variants (typically referred to as morphotypes as they are identified based on distinct colony morphology), appears to be very common, especially in structured environments which offer alternative niches varying in nutrient and oxygen content (Martin et al 2016;Steenackers 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). 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).…”

“…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 .…”

“…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).…”