Environmental modification and niche construction: developing O2 gradients drive the evolution of the Wrinkly Spreader

The evolutionary success of the novel Wrinkly Spreader (WS) genotypes in diversifying Pseudomonas fluorescens SBW25 populations in static liquid microcosms has been attributed to the greater availability of O-2 at the air-liquid (A-L) interface where the WS produces a physically cohesive-class biofilm. However, the importance of O-2 gradients in SBW25 adaptation has never been examined. We have explicitly tested the role of O-2 in evolving populations using microsensor profiling and experiments conducted under high and low O-2 conditions. Initial colonists of static microcosms were found to establish O-2 gradients before significant population growth had occurred, converting a previously homogenous environment into one containing a resource continuum with high and low O-2 regions. These gradients were found to persist for long periods by which time significant numbers of WS had appeared colonising the high O-2 niches. Growth was O-2 limited in static microcosms, but high O-2 conditions like those found near the A-L interface supported greater growth and favoured the emergence of WS-like genotypes. A fitness advantage to biofilm formation was seen under high but not low O-2 conditions, suggesting that the cost of biofilm production could only be offset when O-2 levels above the A-L interface were high. Profiling of mature WS biofilms showed that they also contained high and low O-2 regions. Niches within these may support further diversification and succession of the developing biofilm population. O-2 availability has been found to be a major factor underlying the evolutionary success of the WS genotype in static microcosms and illustrates the importance of this resource continuum in microbial diversification and adaptation. The ISME Journal (2011) 5, 665-673; doi:10.1038/ismej.2010.156; published online 21 October 2010