Adaptive Divergence in Experimental Populations ofPseudomonas fluorescens. V. Insight into the Niche Specialist Fuzzy Spreader Compels Revision of the ModelPseudomonasRadiation

Abstract

Pseudomonas fluorescens is a model for the study of adaptive radiation. When propagated in a spatially structured environment, the bacterium rapidly diversifies into a range of niche specialist genotypes. Here we present a genetic dissection and phenotypic characterization of the fuzzy spreader (FS) morphotype-a type that arises repeatedly during the course of the P. fluorescens radiation and appears to colonize the bottom of static broth microcosms. The causal mutation is located within gene fuzY (pflu0478)-the fourth gene of the five-gene fuzVWXYZ operon. fuzY encodes a b-glycosyltransferase that is predicted to modify lipopolysaccharide (LPS) O antigens. The effect of the mutation is to cause cell flocculation. Analysis of 92 independent FS genotypes showed each to have arisen as the result of a loss-of-function mutation in fuzY, although different mutations have subtly different phenotypic and fitness effects. Mutations within fuzY were previously shown to suppress the phenotype of mat-forming wrinkly spreader (WS) types. This prompted a reinvestigation of FS niche preference. Time-lapse photography showed that FS colonizes the meniscus of broth microcosms, forming cellular rafts that, being too flimsy to form a mat, collapse to the vial bottom and then repeatably reform only to collapse. This led to a reassessment of the ecology of the P. fluorescens radiation. Finally, we show that ecological interactions between the three dominant emergent types (smooth, WS, and FS), combined with the interdependence of FS and WS on fuzY, can, at least in part, underpin an evolutionary arms race with bacteriophage SBW25F2, to which mutation in fuzY confers resistance.A DAPTIVE radiation-the rapid emergence of phenotypic and ecological diversity within an expanding lineage-is among the most striking of evolutionary phenomena (Darwin 1859;Lack 1947;Dobzhansky 1951;Simpson 1953;Schluter 2000;Kassen 2009;Losos 2010). Fueled by competition and facilitated by ecological opportunity, successive radiations have shaped much of life's diversity. Of central importance are the phenotypic innovations that fashion the fit between organism and environment (Schluter 2000).Understanding the nature of these innovations and the pathways by which they emerge and rise to prominenceoften in parallel across estranged populations experiencing similar environments-is a central issue (Colosimo et al. 2005;Bantinaki et al. 2007;Conte et al. 2012). How mutational processes generate the variation presented to selection (McDonald et al. 2009;Braendle et al. 2010), how genetic architecture underpinning extant phenotypes determines the capacity of lineages to generate new and adaptive phenotypes (Poole et al. 2003;Wagner and Zhang 2011), and how ecological factors drive phenotypic divergence (Schluter 2009) are questions of seminal interest.The relative simplicity of microbial systems, their capacity for rapid evolutionary change, and advances in technology that enable detailed genotypic traceability offer a unique opportunity to log moment-by-...

Founder niche constrains evolutionary adaptive radiation

“…SM and WS genotypes appear to correspond to two potentially overlapping clusters in niche space. Recent work indicates the same holds for the niches of WS and fuzzy spreader genotypes (47).…”

“…Coexistence among WS genotypes has also been shown to be stabilized by negative frequency-dependent fitness interactions, indicating differences between their niches (41). The genetic changes underlying this model of adaptive radiation have been established for various niche specialists at the nucleotide level (40,(42)(43)(44)(45)(46)(47).…”

Evolutionary convergence in experimental Pseudomonas populations

“…Diversification of SM SBW25 (Figure 4a) showed a typical pattern with WS arising on day 3 and Fuzzy Spreader (FS) types at day 4 (Ferguson et al, 2013). Interestingly, CC types were detected on day 1 but never increased beyond a small fraction.…”

Trophic regulation of autoaggregation in Pseudomonas taiwanensis VLB120

“…When a mixture of carbon sources was offered (glucose and citrate; glucose and tryptone), no aggregation was observed. As earlier studies reported an influence of the pH on the aggregate formation (Ferguson et al 2013), glucose-containing media were tested in the pH range of 6.4-8.0. Here, no effect of the pH on the aggregation behaviour of the Fig.…”