title: Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models.
abstract: As biofilms grow, resident cells inevitably face the challenge of resource limitation. In the opportunistic pathogen Pseudomonas aeruginosa PA14, electron acceptor availability affects matrix production and, as a result, biofilm morphogenesis. The secreted matrix polysaccharide Pel is required for pellicle formation and for colony wrinkling, two activities that promote access to O2. We examined the exploitability and evolvability of Pel production at the air-liquid interface (during pellicle formation) and on solid surfaces (during colony formation). Although Pel contributes to the developmental response to electron acceptor limitation in both biofilm formation regimes, we found variation in the exploitability of its production and necessity for competitive fitness between the two systems. The wild type showed a competitive advantage against a non-Pel-producing mutant in pellicles but no advantage in colonies. Adaptation to the pellicle environment selected for mutants with a competitive advantage against the wild type in pellicles but also caused a severe disadvantage in colonies, even in wrinkled colony centers. Evolution in the colony center produced divergent phenotypes, while adaptation to the colony edge produced mutants with clear competitive advantages against the wild type in this O2-replete niche. In general, the structurally heterogeneous colony environment promoted more diversification than the more homogeneous pellicle. These results suggest that the role of Pel in community structure formation in response to electron acceptor limitation is unique to specific biofilm models and that the facultative control of Pel production is required for PA14 to maintain optimum benefit in different types of communities.
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA Department of Biology, University of Copenhagen, Copenhagen, Denmark.
authors.forename: Jonas S
authors.initials: JS
authors.lastname: Madsen
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA.
authors.forename: Yu-Cheng
authors.initials: YC
authors.lastname: Lin
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA.
authors.forename: Georgia R
authors.initials: GR
authors.lastname: Squyres
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA.
authors.forename: Alexa
authors.initials: A
authors.lastname: Price-Whelan
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA.
authors.forename: Ana
authors.initials: A
authors.lastname: de Santiago Torio
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA.
authors.forename: Angela
authors.initials: A
authors.lastname: Song
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA.
authors.forename: William C
authors.initials: WC
authors.lastname: Cornell
authors.affiliation: Department of Biology, University of Copenhagen, Copenhagen, Denmark.
authors.forename: Søren J
authors.initials: SJ
authors.lastname: Sørensen
authors.affiliation: Program in Computational Biology, Memorial Sloan-Kettering Cancer Center, New York, New York, USA XavierJ@mskcc.org LDietrich@columbia.edu.
authors.forename: Joao B
authors.initials: JB
authors.lastname: Xavier
authors.affiliation: Department of Biological Sciences, Columbia University, New York, New York, USA XavierJ@mskcc.org LDietrich@columbia.edu.
authors.forename: Lars E P
authors.identifier: http://orcid.org/0000-0003-2049-1137
authors.initials: LE
authors.lastname: Dietrich
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D018441:Biofilms / Q000254:growth & development*; D015964:Gene Expression Regulation, Bacterial; D056265:Microbial Interactions / Q000235:genetics*; D010641:Phenotype; D011135:Polysaccharides, Bacterial / Q000096:biosynthesis*; D011550:Pseudomonas aeruginosa / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism*
chemical_list: D001426:Bacterial Proteins; D011135:Polysaccharides, Bacterial