The Evolution of Quorum Sensing in Bacterial Biofilms
Publication Date
January 29, 2008
Journal
PLOS Biology
Authors
Carey D Nadell, Joao B Xavier, Simon A Levin & Kevin R Foster
Volume
6
Issue
1
Pages
e14
DOI
https://dx.plos.org/10.1371/journal.pbio.0060014
Publisher URL
http://journals.plos.org/plosbiology/article?id=10.1371%2Fjournal.pbio.0060014
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/18232735
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2214811
Europe PMC
http://europepmc.org/abstract/MED/18232735
Web of Science
000254928300016
Scopus
38949209540
Mendeley
http://www.mendeley.com/research/evolution-quorum-sensing-bacterial-biofilms
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CiteULike | Further Information

Mendeley | Further Information

{"title"=>"The evolution of quorum sensing in bacterial biofilms", "type"=>"journal", "authors"=>[{"first_name"=>"Carey D.", "last_name"=>"Nadell", "scopus_author_id"=>"23490155000"}, {"first_name"=>"Joao B.", "last_name"=>"Xavier", "scopus_author_id"=>"55220759500"}, {"first_name"=>"Simon A.", "last_name"=>"Levin", "scopus_author_id"=>"26643470900"}, {"first_name"=>"Kevin R.", "last_name"=>"Foster", "scopus_author_id"=>"7202155866"}], "year"=>2008, "source"=>"PLoS Biology", "identifiers"=>{"isbn"=>"1544-9173", "scopus"=>"2-s2.0-38949209540", "pui"=>"351226055", "doi"=>"10.1371/journal.pbio.0060014", "issn"=>"15449173", "pmid"=>"18232735", "sgr"=>"38949209540"}, "id"=>"53cf104b-956a-3dd6-af00-a730a0b93ec6", "abstract"=>"Bacteria have fascinating and diverse social lives. They display coordinated group behaviors regulated by quorum-sensing systems that detect the density of other bacteria around them. A key example of such group behavior is biofilm formation, in which communities of cells attach to a surface and envelope themselves in secreted polymers. Curiously, after reaching high cell density, some bacterial species activate polymer secretion, whereas others terminate polymer secretion. Here, we investigate this striking variation in the first evolutionary model of quorum sensing in biofilms. We use detailed individual-based simulations to investigate evolutionary competitions between strains that differ in their polymer production and quorum-sensing phenotypes. The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells. But why use quorum sensing to terminate polymer secretion at high cell density? We find that deactivating polymer production in biofilms can yield an advantage by redirecting resources into growth, but that this advantage occurs only in a limited time window. We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains. Our model suggests that the observed variation in quorum-sensing behavior can be linked to the differing requirements of bacteria in chronic versus acute biofilm infections. This is well illustrated by the case of Vibrio cholerae, which competes within biofilms by polymer secretion, terminates polymer secretion at high cell density, and induces an acute disease course that ends with mass dispersal from the host. More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing.", "link"=>"http://www.mendeley.com/research/evolution-quorum-sensing-bacterial-biofilms", "reader_count"=>582, "reader_count_by_academic_status"=>{"Unspecified"=>10, "Professor > Associate Professor"=>34, "Researcher"=>136, "Student > Doctoral Student"=>18, "Student > Ph. D. Student"=>177, "Student > Postgraduate"=>33, "Other"=>18, "Student > Master"=>60, "Student > Bachelor"=>55, "Lecturer"=>6, "Lecturer > Senior Lecturer"=>5, "Professor"=>30}, "reader_count_by_user_role"=>{"Unspecified"=>10, "Professor > Associate Professor"=>34, "Researcher"=>136, "Student > Doctoral Student"=>18, "Student > Ph. D. Student"=>177, "Student > Postgraduate"=>33, "Other"=>18, "Student > Master"=>60, "Student > Bachelor"=>55, "Lecturer"=>6, "Lecturer > Senior Lecturer"=>5, "Professor"=>30}, "reader_count_by_subject_area"=>{"Unspecified"=>26, "Agricultural and Biological Sciences"=>350, "Philosophy"=>1, "Veterinary Science and Veterinary Medicine"=>2, "Chemical Engineering"=>2, "Chemistry"=>23, "Computer Science"=>13, "Earth and Planetary Sciences"=>4, "Engineering"=>21, "Environmental Science"=>24, "Biochemistry, Genetics and Molecular Biology"=>46, "Materials Science"=>4, "Mathematics"=>4, "Medicine and Dentistry"=>19, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>3, "Physics and Astronomy"=>15, "Psychology"=>1, "Immunology and Microbiology"=>21, "Linguistics"=>2}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>4}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>19}, "Physics and Astronomy"=>{"Physics and Astronomy"=>15}, "Psychology"=>{"Psychology"=>1}, "Mathematics"=>{"Mathematics"=>4}, "Unspecified"=>{"Unspecified"=>26}, "Environmental Science"=>{"Environmental Science"=>24}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>3}, "Chemical Engineering"=>{"Chemical Engineering"=>2}, "Engineering"=>{"Engineering"=>21}, "Chemistry"=>{"Chemistry"=>23}, "Neuroscience"=>{"Neuroscience"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>4}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>21}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>350}, "Computer Science"=>{"Computer Science"=>13}, "Linguistics"=>{"Linguistics"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>46}, "Philosophy"=>{"Philosophy"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"Argentina"=>1, "Hungary"=>1, "United States"=>25, "United Kingdom"=>8, "Kenya"=>1, "Switzerland"=>4, "Spain"=>4, "India"=>3, "Greece"=>1, "Canada"=>2, "Austria"=>1, "Pakistan"=>1, "Belgium"=>2, "China"=>1, "Taiwan"=>1, "Poland"=>1, "Brazil"=>3, "Mexico"=>1, "Italy"=>2, "France"=>2, "Chile"=>5, "Germany"=>5}, "group_count"=>21}

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/462434", "https://ndownloader.figshare.com/files/462559", "https://ndownloader.figshare.com/files/462701", "https://ndownloader.figshare.com/files/462787"], "description"=>"<div><p>Bacteria have fascinating and diverse social lives. They display coordinated group behaviors regulated by quorum-sensing systems that detect the density of other bacteria around them. A key example of such group behavior is biofilm formation, in which communities of cells attach to a surface and envelope themselves in secreted polymers. Curiously, after reaching high cell density, some bacterial species activate polymer secretion, whereas others terminate polymer secretion. Here, we investigate this striking variation in the first evolutionary model of quorum sensing in biofilms. We use detailed individual-based simulations to investigate evolutionary competitions between strains that differ in their polymer production and quorum-sensing phenotypes. The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells. But why use quorum sensing to <em>terminate</em> polymer secretion at high cell density? We find that deactivating polymer production in biofilms can yield an advantage by redirecting resources into growth, but that this advantage occurs only in a limited time window. We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains. Our model suggests that the observed variation in quorum-sensing behavior can be linked to the differing requirements of bacteria in chronic versus acute biofilm infections. This is well illustrated by the case of Vibrio cholerae, which competes within biofilms by polymer secretion, terminates polymer secretion at high cell density, and induces an acute disease course that ends with mass dispersal from the host. More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing.</p> </div>", "links"=>[], "tags"=>["quorum", "sensing", "bacterial", "biofilms"], "article_id"=>151144, "categories"=>["Microbiology", "Evolutionary Biology"], "users"=>["Carey D Nadell", "João B Xavier", "Simon A Levin", "Kevin R Foster"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.0060014.sg001", "https://dx.doi.org/10.1371/journal.pbio.0060014.sg002", "https://dx.doi.org/10.1371/journal.pbio.0060014.sd001", "https://dx.doi.org/10.1371/journal.pbio.0060014.sv001"], "stats"=>{"downloads"=>69, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Evolution_of_Quorum_Sensing_in_Bacterial_Biofilms/151144", "title"=>"The Evolution of Quorum Sensing in Bacterial Biofilms", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-01-29 00:19:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/938847"], "description"=>"<div><p>Invasiveness of a rare mutant was analyzed for different degrees of mixing among strains in biofilms, reflected in the different initial frequencies of the rare strain in the biofilm. For example, if 10 strains are randomly sampled, then the initial frequency of the rare mutant in its own biofilm will be 0.1; initial relatedness will also be 0.1 (see main text). Each box and whisker plot summarizes the results of 20 replicate simulations, and plus signs (+) denote outliers. All simulations were carried out at α = 0.008 for the QS<sup>+</sup> strain.</p>\n <p>(A) Invasion of a rare quorum-sensing strain (QS<sup>+</sup>) into a population of unconditional EPS producers (EPS<sup>+</sup>), and (B) failure of a rare EPS<sup>+</sup> strain to invade a population of QS<sup>+</sup> bacteria. Biofilms composed entirely of QS<sup>+</sup> cells attain higher average fitness than biofilms composed entirely of EPS<sup>+</sup> cells.</p>\n <p>(C) Invasion of a rare QS<sup>+</sup> strain into a population of non-EPS producers (EPS<sup>−</sup>), and (D) failure of a rare EPS<sup>−</sup> strain to invade a population of QS<sup>+</sup> bacteria. Again, the QS<sup>+</sup> strain can invade EPS<sup>−</sup>, whereas EPS<sup>−</sup> cannot invade QS<sup>+</sup>. Notably, however, biofilms composed entirely of QS<sup>+</sup> cells have a lower average fitness than biofilms composed entirely of EPS<sup>−</sup> cells. Therefore, if all biofilms contained only a single genotype (no within-biofilm evolutionary competition), the EPS<sup>−</sup> would invade and resist invasion.</p></div>", "links"=>[], "tags"=>["quorum-sensing", "non-quorum-sensing", "vice"], "article_id"=>609289, "categories"=>["Microbiology", "Evolutionary Biology"], "users"=>["Carey D Nadell", "João B Xavier", "Simon A Levin", "Kevin R Foster"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0060014.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Quorum_Sensing_Strain_Can_Invade_Non_Quorum_Sensing_Strains_but_Not_Vice_Versa_/609289", "title"=>"The Quorum-Sensing Strain Can Invade Non-Quorum-Sensing Strains, but Not Vice Versa", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 02:34:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/938707"], "description"=>"<p>Autoinducer (AI) concentration is shown in the background, where isoconcentration lines represent 0.1-mg/l steps. Both strains behave identically, producing both EPS and biomass, until the autoinducer quorum-sensing threshold is reached. QS<sup>+</sup> cells then turn off polymer secretion, devote all resources to biomass production, and achieve a growth burst at locations on the upper surface of the biofilm where substrate availability is highest. A movie for this simulation is provided as <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.0060014#pbio-0060014-sv001\" target=\"_blank\">Video S1</a>.</p>", "links"=>[], "tags"=>["initialized", "numbers"], "article_id"=>609155, "categories"=>["Microbiology", "Evolutionary Biology"], "users"=>["Carey D Nadell", "João B Xavier", "Simon A Levin", "Kevin R Foster"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0060014.g001", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Direct_Competition_between_QS_and_EPS_Bacteria_Initialized_with_Equal_Numbers_of_Both_Strains_/609155", "title"=>"Direct Competition between QS<sup>+</sup> and EPS<sup>+</sup> Bacteria Initialized with Equal Numbers of Both Strains", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 02:32:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/938766"], "description"=>"<div><p>(A) A quorum-sensing strain that down-regulates polymer secretion at high cell-density (QS<sup>+</sup>) is competed against a constitutive polymer-secreting strain (EPS<sup>+</sup>).</p>\n <p>(B) QS<sup>+</sup> versus non-polymer producer (EPS<sup>−</sup>). Each competition (QS<sup>+</sup> vs. EPS<sup>+</sup>, and QS<sup>+</sup> vs. EPS<sup>−</sup>) was replicated 50 times for each of the α values: ∞, 0.01, 0.008, 0.005, and 0.001, where α captures how quickly the QS<sup>+</sup> strain will switch from low to high cell-density state (see main text). For higher α, QS<sup>+</sup> bacteria will reach their quorum at higher cell density, relatively later on during biofilm growth. Plotted lines represent mean QS<sup>+</sup> frequency time series from each set of 50 simulations and are shown with shaded 95% confidence intervals. Note that in (A) and (B), the plotted lines corresponding to α = ∞ are control treatments in which QS<sup>+</sup> behaves identically to EPS<sup>+</sup> throughout simulations because autoinducer concentrations never reach the QS<sup>+</sup> quorum-sensing threshold. Similarly, in (A) and (B), the plotted lines corresponding to α = 0.001 are control treatments in which QS<sup>+</sup> behaves identically to EPS<sup>−</sup> throughout simulations because autoinducer concentrations always exceed the QS<sup>+</sup> quorum-sensing threshold.</p></div>", "links"=>[], "tags"=>["Evolutionary biology", "microbiology"], "article_id"=>609214, "categories"=>["Microbiology", "Evolutionary Biology"], "users"=>["Carey D Nadell", "João B Xavier", "Simon A Levin", "Kevin R Foster"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0060014.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_Simple_Competitions_/609214", "title"=>"Summary of Simple Competitions", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 02:33:34"}

PMC Usage Stats | Further Information

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Relative Metric

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