Adaptive radiation of Pseudomonas fluorescens SBW25 in experimental microcosms provides an understanding of the evolutionary ecology and molecular biology of A-L interface biofilm formation

Abstract

Combined experimental evolutionary and molecular biology approaches have been used to investigate the adaptive radiation of Pseudomonas fluorescens SBW25 in static microcosms leading to the colonisation of the air-liquid interface by biofilm-forming mutants such as the Wrinkly Spreader (WS). In these microcosms, the ecosystem engineering of the early wild-type colonists establishes the niche space for subsequent WS evolution and colonisation. Random WS mutations occurring in the developing population that deregulate diguanylate cyclases and c-di-GMP homeostasis result in cellulose-based biofilms at the air-liquid interface. These structures allow Wrinkly Spreaders to intercept O2 diffusing into the liquid column and limit the growth of competitors lower down. As the biofilm matures, competition increasingly occurs between WS lineages, and niche divergence within the biofilm may support further diversification before system failure when the structure finally sinks. A combination of pleiotropic and epistasis effects, as well as secondary mutations, may explain variations in WS phenotype and fitness. Understanding how mutations subvert regulatory networks to express intrinsic genome potential and key innovations providing a selective advantage in novel environments is key to understanding the versatility of bacteria, and how selection and ecological opportunity can rapidly lead to substantive changes in phenotype and in community structure and function.

Symbiont evolution during the free-living phase can improve host colonization

“…The pellicle tensile strength data (Fig. S3) demonstrate clearly that biofilm evolution in V. fischeri can lead to ecosystem engineering and niche construction [38,84].…”

“…Environmental gradients will form along surfaces such as sediment, suspended debris, marine snow and detritus. These environmental gradients will foster bacterial aggregations and biofilms at liquid-solid interfaces, which in turn will drive the ecological diversification and biofilm evolution that can facilitate host-microbe interactions [39,83,84].…”

Visualization and characterization of Pseudomonas syringae pv. tomato DC3000 pellicles

“…However, although the matrix of these biofilms is composed mainly of cellulose, this exopolysaccharide is not essential since a mutant unable to synthesize cellulose ( wssBC ) can also form pellicles, although with a very different appearance and consistency (Pérez‐Mendoza et al ., ; this work). Likewise, P. fluorescens SBW25 is able to produce different types of A‐L biofilms with distinct phenotypes depending on the biofilm matrix components, and the wrinkly spreader biofilm, which utilizes cellulose as the primary matrix component, is the most robust and well‐attached biofilm (Koza et al ., ). We should mention that Pto DC3000 lacks the pgaABCD operon involved in the synthesis of PGA in SBW25.…”

“…nutrient) phases (Davey and O'Toole, ; Koza et al ., ; Nait Chabane et al ., ). The requirements for the formation of this type of biofilm are also cell contacts, exopolysaccharide accumulation and, in addition, the ability to growth in static conditions (Friedman and Kolter, ; Ude et al ., ; Robertson et al ., ; Koza et al ., ). A‐L biofilms form more complex structures and require a higher level of organization, compared with S‐L biofilms, owing to the lack of a solid surface on which the growth can be initiated (Branda et al ., ).…”

Nonlinear rheological characteristics of single species bacterial biofilms

“…Rheological tests on this particular species of biofilms have not been performed to the best of our knowledge. In P. fluorescens, the biofilms consist of an acetylated form of cellulose fibre, together with lipo-polysachharides, fibrils and attachment factors like PNAG (poly-N-acetylglucosamine); which provide structural integrity to the wrinkly spreader biofilms 75,76 . Functional amyloids produced by the fap operon have been found to modulate the hydrophobicity of P. fluorescens biofilms and also confer mechanical strength 77 .…”