Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria
Most bacteria in nature live in surface-associated communities rather than planktonic populations. Nonetheless, how surface-associated environments shape bacterial evolutionary adaptation remains poorly understood. Here, we show that subjecting Pseudomonas aeruginosa to repeated rounds of swarming,...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2013-08-01
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| Series: | Cell Reports |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124713003884 |
| _version_ | 1811316025899089920 |
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| author | Dave van Ditmarsch Kerry E. Boyle Hassan Sakhtah Jennifer E. Oyler Carey D. Nadell Éric Déziel Lars E.P. Dietrich Joao B. Xavier |
| author_facet | Dave van Ditmarsch Kerry E. Boyle Hassan Sakhtah Jennifer E. Oyler Carey D. Nadell Éric Déziel Lars E.P. Dietrich Joao B. Xavier |
| author_sort | Dave van Ditmarsch |
| collection | DOAJ |
| description | Most bacteria in nature live in surface-associated communities rather than planktonic populations. Nonetheless, how surface-associated environments shape bacterial evolutionary adaptation remains poorly understood. Here, we show that subjecting Pseudomonas aeruginosa to repeated rounds of swarming, a collective form of surface migration, drives remarkable parallel evolution toward a hyperswarmer phenotype. In all independently evolved hyperswarmers, the reproducible hyperswarming phenotype is caused by parallel point mutations in a flagellar synthesis regulator, FleN, which locks the naturally monoflagellated bacteria in a multiflagellated state and confers a growth rate-independent advantage in swarming. Although hyperswarmers outcompete the ancestral strain in swarming competitions, they are strongly outcompeted in biofilm formation, which is an essential trait for P. aeruginosa in environmental and clinical settings. The finding that evolution in swarming colonies reliably produces evolution of poor biofilm formers supports the existence of an evolutionary trade-off between motility and biofilm formation. |
| first_indexed | 2024-04-13T11:41:36Z |
| format | Article |
| id | doaj.art-4fc5e68d51cc4ad89bbd7b85b48f9979 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-13T11:41:36Z |
| publishDate | 2013-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-4fc5e68d51cc4ad89bbd7b85b48f99792022-12-22T02:48:17ZengElsevierCell Reports2211-12472013-08-014469770810.1016/j.celrep.2013.07.026Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic BacteriaDave van Ditmarsch0Kerry E. Boyle1Hassan Sakhtah2Jennifer E. Oyler3Carey D. Nadell4Éric Déziel5Lars E.P. Dietrich6Joao B. Xavier7Program in Computational Biology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USAProgram in Computational Biology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USADepartment of Biological Sciences, Columbia University, 1108 Fairchild Center, 1212 Amsterdam Avenue, Mail Code 2418, New York, NY 10027, USAProgram in Computational Biology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USADepartment of Molecular Biology, Princeton University, Princeton, NJ 08544, USAINRS-Institut Armand-Frappier, 531 Boulevard des Prairies, Laval, QC H7V 1B7, CanadaDepartment of Biological Sciences, Columbia University, 1108 Fairchild Center, 1212 Amsterdam Avenue, Mail Code 2418, New York, NY 10027, USAProgram in Computational Biology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USAMost bacteria in nature live in surface-associated communities rather than planktonic populations. Nonetheless, how surface-associated environments shape bacterial evolutionary adaptation remains poorly understood. Here, we show that subjecting Pseudomonas aeruginosa to repeated rounds of swarming, a collective form of surface migration, drives remarkable parallel evolution toward a hyperswarmer phenotype. In all independently evolved hyperswarmers, the reproducible hyperswarming phenotype is caused by parallel point mutations in a flagellar synthesis regulator, FleN, which locks the naturally monoflagellated bacteria in a multiflagellated state and confers a growth rate-independent advantage in swarming. Although hyperswarmers outcompete the ancestral strain in swarming competitions, they are strongly outcompeted in biofilm formation, which is an essential trait for P. aeruginosa in environmental and clinical settings. The finding that evolution in swarming colonies reliably produces evolution of poor biofilm formers supports the existence of an evolutionary trade-off between motility and biofilm formation.http://www.sciencedirect.com/science/article/pii/S2211124713003884 |
| spellingShingle | Dave van Ditmarsch Kerry E. Boyle Hassan Sakhtah Jennifer E. Oyler Carey D. Nadell Éric Déziel Lars E.P. Dietrich Joao B. Xavier Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria Cell Reports |
| title | Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria |
| title_full | Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria |
| title_fullStr | Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria |
| title_full_unstemmed | Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria |
| title_short | Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria |
| title_sort | convergent evolution of hyperswarming leads to impaired biofilm formation in pathogenic bacteria |
| url | http://www.sciencedirect.com/science/article/pii/S2211124713003884 |
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