Autoinducers act as biological timers in Vibrio harveyi
Quorum sensing regulates cell density-dependent phenotypes and involves the synthesis, excretion and detection of so-called autoinducers. Vibrio harveyi strain ATCC BAA-1116 (recently reclassified as Vibrio campbellii), one of the best-characterized model organisms for the study of quorum sensing, p...
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| creator | Anetzberger, Claudia Reiger, Matthias Fekete, Agnes Schell, Ursula Stambrau, Nina Plener, Laure Kopka, Joachim Schmitt-Kopplin, Phillippe Hilbi, Hubert Jung, Kirsten |
| description | Quorum sensing regulates cell density-dependent phenotypes and involves the synthesis, excretion and detection of so-called autoinducers. Vibrio harveyi strain ATCC BAA-1116 (recently reclassified as Vibrio campbellii), one of the best-characterized model organisms for the study of quorum sensing, produces and responds to three autoinducers. HAI-1, AI-2 and CAI-1 are recognized by different receptors, but all information is channeled into the same signaling cascade, which controls a specific set of genes. Here we examine temporal variations of availability and concentration of the three autoinducers in V. harveyi, and monitor the phenotypes they regulate, from the early exponential to the stationary growth phase in liquid culture. Specifically, the exponential growth phase is characterized by an increase in AI-2 and the induction of bioluminescence, while HAI-1 and CAI-1 are undetectable prior to the late exponential growth phase. CAI-1 activity reaches its maximum upon entry into stationary phase, while molar concentrations of AI-2 and HAI-1 become approximately equal. Similarly, autoinducer-dependent exoproteolytic activity increases at the transition into stationary phase. These findings are reflected in temporal alterations in expression of the luxR gene that encodes the master regulator LuxR, and of four autoinducer-regulated genes during growth. Moreover, in vitro phosphorylation assays reveal a tight correlation between the HAI-1/AI-2 ratio as input and levels of receptor-mediated phosphorylation of LuxU as output. Our study supports a model in which the combinations of autoinducers available, rather than cell density per se, determine the timing of various processes in V. harveyi populations. |
| doi_str_mv | 10.1371/journal.pone.0048310 |
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Vibrio harveyi strain ATCC BAA-1116 (recently reclassified as Vibrio campbellii), one of the best-characterized model organisms for the study of quorum sensing, produces and responds to three autoinducers. HAI-1, AI-2 and CAI-1 are recognized by different receptors, but all information is channeled into the same signaling cascade, which controls a specific set of genes. Here we examine temporal variations of availability and concentration of the three autoinducers in V. harveyi, and monitor the phenotypes they regulate, from the early exponential to the stationary growth phase in liquid culture. Specifically, the exponential growth phase is characterized by an increase in AI-2 and the induction of bioluminescence, while HAI-1 and CAI-1 are undetectable prior to the late exponential growth phase. CAI-1 activity reaches its maximum upon entry into stationary phase, while molar concentrations of AI-2 and HAI-1 become approximately equal. Similarly, autoinducer-dependent exoproteolytic activity increases at the transition into stationary phase. These findings are reflected in temporal alterations in expression of the luxR gene that encodes the master regulator LuxR, and of four autoinducer-regulated genes during growth. Moreover, in vitro phosphorylation assays reveal a tight correlation between the HAI-1/AI-2 ratio as input and levels of receptor-mediated phosphorylation of LuxU as output. Our study supports a model in which the combinations of autoinducers available, rather than cell density per se, determine the timing of various processes in V. harveyi populations.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0048310</identifier><identifier>PMID: 23110227</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bacterial Proteins - metabolism ; Biochemistry ; Biofilms ; Biology ; Bioluminescence ; Cell culture ; Cell density ; Cooperation ; E coli ; Enzymes ; Escherichia coli ; Excretion ; Gene expression ; Gene Expression Regulation, Bacterial ; Genes ; Kinases ; Liquid culture ; Phase transitions ; Phosphorylation ; Proteins ; Quorum Sensing - physiology ; Receptors ; Science ; Sensors ; Signaling ; Stationary phase ; Temporal variations ; Timing devices ; Vibrio - metabolism ; Vibrio - physiology ; Vibrio cholerae ; Vibrio harveyi ; Water-borne diseases ; Waterborne diseases</subject><ispartof>PloS one, 2012-10, Vol.7 (10), p.e48310-e48310</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Anetzberger et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2012 Anetzberger et al 2012 Anetzberger et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-78d51d3056fe49e34a73fe58e227e5b33b06d3436340c19ae364c3c78cda91d33</citedby><cites>FETCH-LOGICAL-c758t-78d51d3056fe49e34a73fe58e227e5b33b06d3436340c19ae364c3c78cda91d33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3482212/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3482212/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2101,2927,23865,27923,27924,53790,53792,79471,79472</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23110227$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Misra, Rajeev</contributor><creatorcontrib>Anetzberger, Claudia</creatorcontrib><creatorcontrib>Reiger, Matthias</creatorcontrib><creatorcontrib>Fekete, Agnes</creatorcontrib><creatorcontrib>Schell, Ursula</creatorcontrib><creatorcontrib>Stambrau, Nina</creatorcontrib><creatorcontrib>Plener, Laure</creatorcontrib><creatorcontrib>Kopka, Joachim</creatorcontrib><creatorcontrib>Schmitt-Kopplin, Phillippe</creatorcontrib><creatorcontrib>Hilbi, Hubert</creatorcontrib><creatorcontrib>Jung, Kirsten</creatorcontrib><title>Autoinducers act as biological timers in Vibrio harveyi</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Quorum sensing regulates cell density-dependent phenotypes and involves the synthesis, excretion and detection of so-called autoinducers. Vibrio harveyi strain ATCC BAA-1116 (recently reclassified as Vibrio campbellii), one of the best-characterized model organisms for the study of quorum sensing, produces and responds to three autoinducers. HAI-1, AI-2 and CAI-1 are recognized by different receptors, but all information is channeled into the same signaling cascade, which controls a specific set of genes. Here we examine temporal variations of availability and concentration of the three autoinducers in V. harveyi, and monitor the phenotypes they regulate, from the early exponential to the stationary growth phase in liquid culture. Specifically, the exponential growth phase is characterized by an increase in AI-2 and the induction of bioluminescence, while HAI-1 and CAI-1 are undetectable prior to the late exponential growth phase. CAI-1 activity reaches its maximum upon entry into stationary phase, while molar concentrations of AI-2 and HAI-1 become approximately equal. Similarly, autoinducer-dependent exoproteolytic activity increases at the transition into stationary phase. These findings are reflected in temporal alterations in expression of the luxR gene that encodes the master regulator LuxR, and of four autoinducer-regulated genes during growth. Moreover, in vitro phosphorylation assays reveal a tight correlation between the HAI-1/AI-2 ratio as input and levels of receptor-mediated phosphorylation of LuxU as output. 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Vibrio harveyi strain ATCC BAA-1116 (recently reclassified as Vibrio campbellii), one of the best-characterized model organisms for the study of quorum sensing, produces and responds to three autoinducers. HAI-1, AI-2 and CAI-1 are recognized by different receptors, but all information is channeled into the same signaling cascade, which controls a specific set of genes. Here we examine temporal variations of availability and concentration of the three autoinducers in V. harveyi, and monitor the phenotypes they regulate, from the early exponential to the stationary growth phase in liquid culture. Specifically, the exponential growth phase is characterized by an increase in AI-2 and the induction of bioluminescence, while HAI-1 and CAI-1 are undetectable prior to the late exponential growth phase. CAI-1 activity reaches its maximum upon entry into stationary phase, while molar concentrations of AI-2 and HAI-1 become approximately equal. Similarly, autoinducer-dependent exoproteolytic activity increases at the transition into stationary phase. These findings are reflected in temporal alterations in expression of the luxR gene that encodes the master regulator LuxR, and of four autoinducer-regulated genes during growth. Moreover, in vitro phosphorylation assays reveal a tight correlation between the HAI-1/AI-2 ratio as input and levels of receptor-mediated phosphorylation of LuxU as output. Our study supports a model in which the combinations of autoinducers available, rather than cell density per se, determine the timing of various processes in V. harveyi populations.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23110227</pmid><doi>10.1371/journal.pone.0048310</doi><tpages>e48310</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Bacterial Proteins - metabolism Biochemistry Biofilms Biology Bioluminescence Cell culture Cell density Cooperation E coli Enzymes Escherichia coli Excretion Gene expression Gene Expression Regulation, Bacterial Genes Kinases Liquid culture Phase transitions Phosphorylation Proteins Quorum Sensing - physiology Receptors Science Sensors Signaling Stationary phase Temporal variations Timing devices Vibrio - metabolism Vibrio - physiology Vibrio cholerae Vibrio harveyi Water-borne diseases Waterborne diseases |
| title | Autoinducers act as biological timers in Vibrio harveyi |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-08T12%3A13%3A41IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Autoinducers%20act%20as%20biological%20timers%20in%20Vibrio%20harveyi&rft.jtitle=PloS%20one&rft.au=Anetzberger,%20Claudia&rft.date=2012-10-26&rft.volume=7&rft.issue=10&rft.spage=e48310&rft.epage=e48310&rft.pages=e48310-e48310&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0048310&rft_dat=%3Cgale_plos_%3EA477034225%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1326561766&rft_id=info:pmid/23110227&rft_galeid=A477034225&rft_doaj_id=oai_doaj_org_article_71b617aaf9dd47e0b22a32f57a090469&rfr_iscdi=true |