Bistability in a metabolic network underpins the De Novo evolution of colony switching in Pseudomonas fluorescens

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dc.citation.issue3
dc.citation.volume13
dc.contributor.authorGallie J
dc.contributor.authorLibby E
dc.contributor.authorBertels F
dc.contributor.authorRemigi P
dc.contributor.authorJendresen CB
dc.contributor.authorFerguson GC
dc.contributor.authorDesprat N
dc.contributor.authorBuffing MF
dc.contributor.authorSauer U
dc.contributor.authorBeaumont HJE
dc.contributor.authorMartinussen J
dc.contributor.authorKilstrup M
dc.contributor.authorRainey PB
dc.date.available2015-03-01
dc.date.available2015-02-18
dc.date.issued2015-03-12
dc.descriptionCreative Commons Attribution license
dc.description.abstract© 2015 Gallie et al. Phenotype switching is commonly observed in nature. This prevalence has allowed the elucidation of a number of underlying molecular mechanisms. However, little is known about how phenotypic switches arise and function in their early evolutionary stages. The first opportunity to provide empirical insight was delivered by an experiment in which populations of the bacterium Pseudomonas fluorescens SBW25 evolved, de novo, the ability to switch between two colony phenotypes. Here we unravel the molecular mechanism behind colony switching, revealing how a single nucleotide change in a gene enmeshed in central metabolism (carB) generates such a striking phenotype. We show that colony switching is underpinned by ON/OFF expression of capsules consisting of a colanic acid-like polymer. We use molecular genetics, biochemical analyses, and experimental evolution to establish that capsule switching results from perturbation of the pyrimidine biosynthetic pathway. Of central importance is a bifurcation point at which uracil triphosphate is partitioned towards either nucleotide metabolism or polymer production. This bifurcation marks a cell-fate decision point whereby cells with relatively high pyrimidine levels favour nucleotide metabolism (capsule OFF), while cells with lower pyrimidine levels divert resources towards polymer biosynthesis (capsule ON). This decision point is present and functional in the wild-type strain. Finally, we present a simple mathematical model demonstrating that the molecular components of the decision point are capable of producing switching. Despite its simple mutational cause, the connection between genotype and phenotype is complex and multidimensional, offering a rare glimpse of how noise in regulatory networks can provide opportunity for evolution.
dc.description.publication-statusPublished
dc.format.extent? - ? (28)
dc.identifierhttp://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000352095700018&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=c5bb3b2499afac691c2e3c1a83ef6fef
dc.identifierARTN e1002109
dc.identifier.citationPLOS BIOLOGY, 2015, 13 (3), pp. ? - ? (28)
dc.identifier.doi10.1371/journal.pbio.1002109
dc.identifier.elements-id223700
dc.identifier.issn1545-7885
dc.languageEnglish
dc.publisherPUBLIC LIBRARY SCIENCE
dc.relation.isPartOfPLOS BIOLOGY
dc.subjectScience & Technology
dc.subjectLife Sciences & Biomedicine
dc.subjectBiochemistry & Molecular Biology
dc.subjectBiology
dc.subjectLife Sciences & Biomedicine - Other Topics
dc.subjectNUCLEOSIDE DIPHOSPHATE KINASE
dc.subjectESCHERICHIA-COLI K-12
dc.subjectCOLANIC ACID
dc.subjectPOLYSACCHARIDE SYNTHESIS
dc.subjectNUCLEOTIDE-METABOLISM
dc.subjectPHOSPHATE SYNTHETASE
dc.subjectPATHOGENIC BACTERIA
dc.subjectGENE-EXPRESSION
dc.subjectENVIRONMENT
dc.subjectAERUGINOSA
dc.subject.anzsrc06 Biological Sciences
dc.subject.anzsrc07 Agricultural and Veterinary Sciences
dc.subject.anzsrc11 Medical and Health Sciences
dc.titleBistability in a metabolic network underpins the De Novo evolution of colony switching in Pseudomonas fluorescens
dc.typeJournal article
pubs.notesNot known
pubs.organisational-group/Massey University
pubs.organisational-group/Massey University/College of Sciences
pubs.organisational-group/Massey University/College of Sciences/School of Natural and Computational Sciences
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