Heterogeneous response to a quorum-sensing signal in the luminescence of individual Vibrio fischeri
The marine bacterium Vibrio fischeri regulates its bioluminescence through a quorum sensing mechanism: the bacterium releases diffusible small molecules (autoinducers) that accumulate in the environment as the population density increases. This accumulation of autoinducer (AI) eventually activates t...
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description | The marine bacterium Vibrio fischeri regulates its bioluminescence through a quorum sensing mechanism: the bacterium releases diffusible small molecules (autoinducers) that accumulate in the environment as the population density increases. This accumulation of autoinducer (AI) eventually activates transcriptional regulators for bioluminescence as well as host colonization behaviors. Although V. fischeri quorum sensing has been extensively characterized in bulk populations, far less is known about how it performs at the level of the individual cell, where biochemical noise is likely to limit the precision of luminescence regulation. We have measured the time-dependence and AI-dependence of light production by individual V. fischeri cells that are immobilized in a perfusion chamber and supplied with a defined concentration of exogenous AI. We use low-light level microscopy to record and quantify the photon emission from the cells over periods of several hours as they respond to the introduction of AI. We observe an extremely heterogeneous response to the AI signal. Individual cells differ widely in the onset time for their luminescence and in their resulting brightness, even in the presence of high AI concentrations that saturate the light output from a bulk population. The observed heterogeneity shows that although a given concentration of quorum signal may determine the average light output from a population of cells, it provides far weaker control over the luminescence output of each individual cell. |
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This accumulation of autoinducer (AI) eventually activates transcriptional regulators for bioluminescence as well as host colonization behaviors. Although V. fischeri quorum sensing has been extensively characterized in bulk populations, far less is known about how it performs at the level of the individual cell, where biochemical noise is likely to limit the precision of luminescence regulation. We have measured the time-dependence and AI-dependence of light production by individual V. fischeri cells that are immobilized in a perfusion chamber and supplied with a defined concentration of exogenous AI. We use low-light level microscopy to record and quantify the photon emission from the cells over periods of several hours as they respond to the introduction of AI. We observe an extremely heterogeneous response to the AI signal. Individual cells differ widely in the onset time for their luminescence and in their resulting brightness, even in the presence of high AI concentrations that saturate the light output from a bulk population. The observed heterogeneity shows that although a given concentration of quorum signal may determine the average light output from a population of cells, it provides far weaker control over the luminescence output of each individual cell.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0015473</identifier><identifier>PMID: 21103327</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aliivibrio fischeri - chemistry ; Aliivibrio fischeri - genetics ; Aliivibrio fischeri - metabolism ; Biology ; Bioluminescence ; Colonization ; Detection ; Gene expression ; Light ; Luminescence ; Luminescent Measurements - instrumentation ; Luminescent Measurements - methods ; Microscopy ; Noise control ; Perfusion ; Photon emission ; Physics ; Population density ; Quorum Sensing - genetics ; Quorum Sensing - physiology ; Regulators ; Signal Transduction - genetics ; Signal Transduction - physiology ; Studies ; Time Factors ; Transcription ; Vibrio ; Vibrio fischeri ; Water-borne diseases ; Waterborne diseases</subject><ispartof>PloS one, 2010-11, Vol.5 (11), p.e15473-e15473</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Pérez, Hagen. 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>Pérez, Hagen. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c723t-1a6dc3cd6d185571a68a3482d7cf83c536d6739c8f76f243b4691e2d204a79f53</citedby><cites>FETCH-LOGICAL-c723t-1a6dc3cd6d185571a68a3482d7cf83c536d6739c8f76f243b4691e2d204a79f53</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/PMC2982848/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2982848/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21103327$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pérez, Pablo Delfino</creatorcontrib><creatorcontrib>Hagen, Stephen J</creatorcontrib><title>Heterogeneous response to a quorum-sensing signal in the luminescence of individual Vibrio fischeri</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The marine bacterium Vibrio fischeri regulates its bioluminescence through a quorum sensing mechanism: the bacterium releases diffusible small molecules (autoinducers) that accumulate in the environment as the population density increases. This accumulation of autoinducer (AI) eventually activates transcriptional regulators for bioluminescence as well as host colonization behaviors. Although V. fischeri quorum sensing has been extensively characterized in bulk populations, far less is known about how it performs at the level of the individual cell, where biochemical noise is likely to limit the precision of luminescence regulation. We have measured the time-dependence and AI-dependence of light production by individual V. fischeri cells that are immobilized in a perfusion chamber and supplied with a defined concentration of exogenous AI. We use low-light level microscopy to record and quantify the photon emission from the cells over periods of several hours as they respond to the introduction of AI. We observe an extremely heterogeneous response to the AI signal. Individual cells differ widely in the onset time for their luminescence and in their resulting brightness, even in the presence of high AI concentrations that saturate the light output from a bulk population. The observed heterogeneity shows that although a given concentration of quorum signal may determine the average light output from a population of cells, it provides far weaker control over the luminescence output of each individual cell.</description><subject>Aliivibrio fischeri - chemistry</subject><subject>Aliivibrio fischeri - genetics</subject><subject>Aliivibrio fischeri - metabolism</subject><subject>Biology</subject><subject>Bioluminescence</subject><subject>Colonization</subject><subject>Detection</subject><subject>Gene expression</subject><subject>Light</subject><subject>Luminescence</subject><subject>Luminescent Measurements - instrumentation</subject><subject>Luminescent Measurements - methods</subject><subject>Microscopy</subject><subject>Noise control</subject><subject>Perfusion</subject><subject>Photon emission</subject><subject>Physics</subject><subject>Population density</subject><subject>Quorum Sensing - genetics</subject><subject>Quorum Sensing - physiology</subject><subject>Regulators</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - physiology</subject><subject>Studies</subject><subject>Time Factors</subject><subject>Transcription</subject><subject>Vibrio</subject><subject>Vibrio fischeri</subject><subject>Water-borne diseases</subject><subject>Waterborne diseases</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk29r2zAQxs3YWLts32BshsHGXiSzdLIkvymUsq2BQmF_-lYo8slRcKxUssv27ae0bolHYcMvbJ1_95z93F2WvSbFgoAgnzZ-CJ1uFzvf4aIoSMkEPMmOSQV0zmkBTw-ej7IXMW6KogTJ-fPsiBJSAFBxnJlz7DH4Bjv0Q8wDxqQXMe99rvPrwYdhO4_YRdc1eXRNKpi7Lu_XmLfD1nUYDXYGc29TuHY3rh4SceVWwfncumjWGNzL7JnVbcRX432W_fzy-cfZ-fzi8uvy7PRibgSFfk40rw2YmtdElqVIR6mBSVoLYyWYEnjNBVRGWsEtZbBivCJIa1owLSpbwix7e6e7a31Uoz9REVrRxHDCErG8I2qvN2oX3FaH38prp24DPjRKh96ZFhUrmECAgttKMtDlygKKsjKUEVbty8-yk7HasNpinXzog24notM3nVurxt8oWkkqmUwCH0aB4K8HjL3aJsOwbfVtL5QUlAAvOf83SRIJFdtb8O4v8nEbRqrR6U9dZ336QLPXVKdpiiTQklaJWjxCpavGrTNp6qxL8UnCx0lCYnr81Td6iFEtv3_7f_byasq-P2DXqNt-HX079C6N6hRkd6AJPsaA9qEbpFD7pbl3Q-2XRo1Lk9LeHHbyIel-S-APA10QuQ</recordid><startdate>20101116</startdate><enddate>20101116</enddate><creator>Pérez, Pablo Delfino</creator><creator>Hagen, Stephen J</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>7TN</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20101116</creationdate><title>Heterogeneous response to a quorum-sensing signal in the luminescence of individual Vibrio fischeri</title><author>Pérez, Pablo Delfino ; Hagen, Stephen J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c723t-1a6dc3cd6d185571a68a3482d7cf83c536d6739c8f76f243b4691e2d204a79f53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Aliivibrio fischeri - 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Academic</collection><collection>Oceanic Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pérez, Pablo Delfino</au><au>Hagen, Stephen J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Heterogeneous response to a quorum-sensing signal in the luminescence of individual Vibrio fischeri</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2010-11-16</date><risdate>2010</risdate><volume>5</volume><issue>11</issue><spage>e15473</spage><epage>e15473</epage><pages>e15473-e15473</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The marine bacterium Vibrio fischeri regulates its bioluminescence through a quorum sensing mechanism: the bacterium releases diffusible small molecules (autoinducers) that accumulate in the environment as the population density increases. This accumulation of autoinducer (AI) eventually activates transcriptional regulators for bioluminescence as well as host colonization behaviors. Although V. fischeri quorum sensing has been extensively characterized in bulk populations, far less is known about how it performs at the level of the individual cell, where biochemical noise is likely to limit the precision of luminescence regulation. We have measured the time-dependence and AI-dependence of light production by individual V. fischeri cells that are immobilized in a perfusion chamber and supplied with a defined concentration of exogenous AI. We use low-light level microscopy to record and quantify the photon emission from the cells over periods of several hours as they respond to the introduction of AI. We observe an extremely heterogeneous response to the AI signal. Individual cells differ widely in the onset time for their luminescence and in their resulting brightness, even in the presence of high AI concentrations that saturate the light output from a bulk population. The observed heterogeneity shows that although a given concentration of quorum signal may determine the average light output from a population of cells, it provides far weaker control over the luminescence output of each individual cell.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21103327</pmid><doi>10.1371/journal.pone.0015473</doi><tpages>e15473</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Aliivibrio fischeri - chemistry Aliivibrio fischeri - genetics Aliivibrio fischeri - metabolism Biology Bioluminescence Colonization Detection Gene expression Light Luminescence Luminescent Measurements - instrumentation Luminescent Measurements - methods Microscopy Noise control Perfusion Photon emission Physics Population density Quorum Sensing - genetics Quorum Sensing - physiology Regulators Signal Transduction - genetics Signal Transduction - physiology Studies Time Factors Transcription Vibrio Vibrio fischeri Water-borne diseases Waterborne diseases |
title | Heterogeneous response to a quorum-sensing signal in the luminescence of individual Vibrio fischeri |
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