The evolution of biofilm-forming Wrinkly Spreaders in static microcosms and drip-fed columns selects for subtle differences in wrinkleality and fitness

Udall, Yvette C.; Deeni, Yusuf Y.; Hapca, Simona M.; Raikes, David

doi:10.1093/femsec/fiv057

Cited by 18 publications

(36 citation statements)

References 41 publications

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“…These environmental conditions include abiotic factors, which have been shown to influence the phenotypic responses of biofilm dispersal isolates. For example, the fitness exhibited by P. fluorescens with wrinkle colony morphologies vaired depending on if grown in environmenally homogenous or heterogenous microcosms (Udall et al, ). However what is less understood is the influence of competing community members toward the development of heretible trait variation on microbial populations.…”

Section: Introductionmentioning

confidence: 99%

Effect of interspecific competition on trait variation in Phaeobacter inhibens biofilms

Lutz¹,

Thomas²,

Steinberg³

et al. 2016

Environmental Microbiology

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Interspecific competition between bacteria shapes community dynamics, causing evolutionary changes that affect life history traits. Here, we studied the role of interspecific competition on the generation of trait diversity using a two-species model system of marine, surface-associated bacteria. Bacterial biofilms of Phaeobacter inhibens were established alone or in competition with Pseudoalteromonas tunicata and phenotypic traits of dispersal cells were assessed during biofilm development. P. inhibens dispersal isolates from competition biofilms displayed less phenotypic variation, were superior competitors, were less susceptible to predation, and reached higher planktonic biomass than isolates from noncompetition biofilms. Moreover, the maintenance of competitive ability exhibited by individual dispersal isolates from competition biofilms did not result in an obvious reduction (measured as a negative trait correlation) in other traits, but was rather positively correlated with planktonic growth. However, where negative correlations between traits were found, they were exhibited by individuals derived from noncompetitive biofilms, whose populations also had a higher degree of trait variation than those from biofilms experiencing competition. Our observations indicate that interspecific competition during biofilm formation is important for maintaining both competitive ability and affects variation in ecologically relevant traits. Given that most bacteria in biofilms exist in diverse, multispecies communities, an understanding of how bacteria respond to biotic factors such as interspecific competition is critical for understanding the dynamics of bacterial populations in both ecological and evolutionary time.

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Section: Introductionmentioning

confidence: 99%

Effect of interspecific competition on trait variation in Phaeobacter inhibens biofilms

Lutz¹,

Thomas²,

Steinberg³

et al. 2016

Environmental Microbiology

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“…Several recent studies have shown that the spatial structure of biofilms has a major impact on competition and cooperation among microbes and drives evolutionary changes within microbial communities (reviewed in refs 4, 5). One particularly well-studied example used static cultures of Pseudomonas fluorescens , where an oxygen gradient led to the emergence of a new wrinkly (W) phenotype that secretes polysaccharides and forms a biofilm at the air–liquid interface67. Interestingly, biofilms formed by W undergo a premature collapse caused by the incorporation of another phenotype into the biofilm without sharing the metabolic costs of exopolymer production8.…”

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confidence: 99%

De novo evolved interference competition promotes the spread of biofilm defectors

et al. 2017

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Biofilms are social entities where bacteria live in tightly packed agglomerations, surrounded by self-secreted exopolymers. Since production of exopolymers is costly and potentially exploitable by non-producers, mechanisms that prevent invasion of non-producing mutants are hypothesized. Here we study long-term dynamics and evolution in Bacillus subtilis biofilm populations consisting of wild-type (WT) matrix producers and mutant non-producers. We show that non-producers initially fail to incorporate into biofilms formed by the WT cells, resulting in 100-fold lower final frequency compared to the WT. However, this is modulated in a long-term scenario, as non-producers evolve the ability to better incorporate into biofilms, thereby slightly decreasing the productivity of the whole population. Detailed molecular analysis reveals that the unexpected shift in the initially stable biofilm is coupled with newly evolved phage-mediated interference competition. Our work therefore demonstrates how collective behaviour can be disrupted as a result of rapid adaptation through mobile genetic elements.

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“…However, Wrinkly Spreaders may also have a maximal population size; as Wrinkly Spreader numbers grow in the maturing biofilm, only the top ~300 µ m layer of the biofilm remains O 2 -rich and lower regions of the biofilm become increasingly O 2 -limited [11]. In this situation, Wrinkly Spreaders start to compete with one another within the biofilm itself, with different WS mutants showing substantial morphological, metabolic, and fitness variation [17, 31–33]. …”

Section: Resultsmentioning

confidence: 99%

New Insights into the Effects of Several Environmental Parameters on the Relative Fitness of a Numerically Dominant Class of Evolved Niche Specialist

Kuśmierska

2016

International Journal of Evolutionary Biology

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Adaptive radiation in bacteria has been investigated using Wrinkly Spreaders (WS), a morphotype which colonises the air-liquid (A-L) interface of static microcosms by biofilm formation with a significant fitness advantage over competitors growing lower down in the O2-limited liquid column. Here, we investigate several environmental parameters which impact the ecological opportunity that the Wrinkly Spreaders exploit in this model system. Manipulation of surface area/volume ratios suggests that the size of the WS niche was not as important as the ability to dominate the A-L interface and restrict competitor growth. The value of this niche to the Wrinkly Spreaders, as determined by competitive fitness assays, was found to increase as O2 flux to the A-L interface was reduced, confirming that competition for O2 was the main driver of WS fitness. The effect of O2 on fitness was also found to be dependent on the availability of nutrients, reflecting the need to take up both for optimal growth. Finally, the meniscus trap, a high-O2 region formed by the interaction of the A-L interface with the vial walls, was also important for fitness during the early stages of biofilm formation. These findings reveal the complexity of this seemingly simple model system and illustrate how changes in environmental physicality alter ecological opportunity and the fitness of the adaptive morphotype.

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The evolution of biofilm-forming Wrinkly Spreaders in static microcosms and drip-fed columns selects for subtle differences in wrinkleality and fitness

Cited by 18 publications

References 41 publications

Effect of interspecific competition on trait variation in Phaeobacter inhibens biofilms

Effect of interspecific competition on trait variation in Phaeobacter inhibens biofilms

De novo evolved interference competition promotes the spread of biofilm defectors

New Insights into the Effects of Several Environmental Parameters on the Relative Fitness of a Numerically Dominant Class of Evolved Niche Specialist

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