Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models

Jonas Stenløkke Madsen; Yu Cheng Lin; Georgia R. Squyres; Alexa Price-Whelan; Ana de Santiago Torio; Angela Song; William C. Cornell; Søren Johannes Sørensen; Joao B. Xavier; Lars E.P. Dietrich

doi:10.1128/aem.02628-15

Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models

Jonas Stenløkke Madsen, Yu Cheng Lin, Georgia R. Squyres, Alexa Price-Whelan, Ana de Santiago Torio, Angela Song, William C. Cornell, Søren Johannes Sørensen, Joao B. Xavier^*, Lars E.P. Dietrich

^*Corresponding author for this work

Microbiology

36 Citations (Scopus)

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.

Original language	English
Journal	Applied and Environmental Microbiology
Volume	81
Issue number	24
Pages (from-to)	8414-8426
Number of pages	13
ISSN	0099-2240
DOIs	https://doi.org/10.1128/aem.02628-15
Publication status	Published - 2015

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Madsen, J. S., Lin, Y. C., Squyres, G. R., Price-Whelan, A., Torio, A. D. S., Song, A., Cornell, W. C., Sørensen, S. J., Xavier, J. B., & Dietrich, L. E. P. (2015). Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models. Applied and Environmental Microbiology, 81(24), 8414-8426. https://doi.org/10.1128/aem.02628-15

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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.",

author = "Madsen, {Jonas Stenl{\o}kke} and Lin, {Yu Cheng} and Squyres, {Georgia R.} and Alexa Price-Whelan and Torio, {Ana de Santiago} and Angela Song and Cornell, {William C.} and S{\o}rensen, {S{\o}ren Johannes} and Xavier, {Joao B.} and Dietrich, {Lars E.P.}",

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doi = "10.1128/aem.02628-15",

language = "English",

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pages = "8414--8426",

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T1 - Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models

AU - Madsen, Jonas Stenløkke

AU - Lin, Yu Cheng

AU - Squyres, Georgia R.

AU - Price-Whelan, Alexa

AU - Torio, Ana de Santiago

AU - Song, Angela

AU - Cornell, William C.

AU - Sørensen, Søren Johannes

AU - Xavier, Joao B.

AU - Dietrich, Lars E.P.

PY - 2015

Y1 - 2015

N2 - 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.

AB - 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.

U2 - 10.1128/aem.02628-15

DO - 10.1128/aem.02628-15

M3 - Journal article

C2 - 26431965

AN - SCOPUS:84949647850

SN - 0099-2240

VL - 81

SP - 8414

EP - 8426

JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

IS - 24

ER -

Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models

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