Biofilm Morphotypes and Population Structure among Staphylococcus epidermidis from Commensal and Clinical Samples
Bacterial species comprise related genotypes that can display divergent phenotypes with important clinical implications. Staphylococcus epidermidis is a common cause of nosocomial infections and, critical to its pathogenesis, is its ability to adhere and form biofilms on surfaces, thereby moderating...
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creator | Harris, Llinos G Murray, Susan Pascoe, Ben Bray, James Meric, Guillaume Mageiros, Leonardos Wilkinson, Thomas S Jeeves, Rose Rohde, Holger Schwarz, Stefan de Lencastre, Herminia Miragaia, Maria Rolo, Joana Bowden, Rory Jolley, Keith A Maiden, Martin C J Mack, Dietrich Sheppard, Samuel K |
description | Bacterial species comprise related genotypes that can display divergent phenotypes with important clinical implications. Staphylococcus epidermidis is a common cause of nosocomial infections and, critical to its pathogenesis, is its ability to adhere and form biofilms on surfaces, thereby moderating the effect of the host's immune response and antibiotics. Commensal S. epidermidis populations are thought to differ from those associated with disease in factors involved in adhesion and biofilm accumulation. We quantified the differences in biofilm formation in 98 S. epidermidis isolates from various sources, and investigated population structure based on ribosomal multilocus typing (rMLST) and the presence/absence of genes involved in adhesion and biofilm formation. All isolates were able to adhere and form biofilms in in vitro growth assays and confocal microscopy allowed classification into 5 biofilm morphotypes based on their thickness, biovolume and roughness. Phylogenetic reconstruction grouped isolates into three separate clades, with the isolates in the main disease associated clade displaying diversity in morphotype. Of the biofilm morphology characteristics, only biofilm thickness had a significant association with clade distribution. The distribution of some known adhesion-associated genes (aap and sesE) among isolates showed a significant association with the species clonal frame. These data challenge the assumption that biofilm-associated genes, such as those on the ica operon, are genetic markers for less invasive S. epidermidis isolates, and suggest that phenotypic characteristics, such as adhesion and biofilm formation, are not fixed by clonal descent but are influenced by the presence of various genes that are mobile among lineages. |
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Staphylococcus epidermidis is a common cause of nosocomial infections and, critical to its pathogenesis, is its ability to adhere and form biofilms on surfaces, thereby moderating the effect of the host's immune response and antibiotics. Commensal S. epidermidis populations are thought to differ from those associated with disease in factors involved in adhesion and biofilm accumulation. We quantified the differences in biofilm formation in 98 S. epidermidis isolates from various sources, and investigated population structure based on ribosomal multilocus typing (rMLST) and the presence/absence of genes involved in adhesion and biofilm formation. All isolates were able to adhere and form biofilms in in vitro growth assays and confocal microscopy allowed classification into 5 biofilm morphotypes based on their thickness, biovolume and roughness. Phylogenetic reconstruction grouped isolates into three separate clades, with the isolates in the main disease associated clade displaying diversity in morphotype. Of the biofilm morphology characteristics, only biofilm thickness had a significant association with clade distribution. The distribution of some known adhesion-associated genes (aap and sesE) among isolates showed a significant association with the species clonal frame. These data challenge the assumption that biofilm-associated genes, such as those on the ica operon, are genetic markers for less invasive S. epidermidis isolates, and suggest that phenotypic characteristics, such as adhesion and biofilm formation, are not fixed by clonal descent but are influenced by the presence of various genes that are mobile among lineages.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0151240</identifier><identifier>PMID: 26978068</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adhesion ; Analysis ; Antibiotics ; Bacteria ; Base sequence ; Biofilms ; Biofilms - classification ; Biofilms - growth & development ; Biology and Life Sciences ; Confocal microscopy ; Consortia ; Cross Infection - microbiology ; Epidemiology ; Gene loci ; Genes ; Genetic aspects ; Genetic markers ; Genetics ; Genomes ; Genomics ; Genotype & phenotype ; Genotypes ; Health aspects ; Hospitals ; Humans ; Immune response ; Immune system ; Infectious diseases ; Laboratories ; Life sciences ; Medical equipment ; Medical schools ; Medicine and Health Sciences ; Microscopy ; Nosocomial infection ; Nosocomial infections ; Pathogenesis ; Phylogeny ; Physical characteristics ; Physiological aspects ; Population structure ; Proteins ; Research and Analysis Methods ; Staphylococcal Infections - microbiology ; Staphylococcus ; Staphylococcus aureus ; Staphylococcus epidermidis ; Staphylococcus epidermidis - genetics ; Staphylococcus infections ; Zoology</subject><ispartof>PloS one, 2016-03, Vol.11 (3), p.e0151240-e0151240</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Harris et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2016 Harris et al 2016 Harris et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-6b85d502e203266ed7515190f3f580a5adb6b51fb46378bf99336669bd1731a63</citedby><cites>FETCH-LOGICAL-c692t-6b85d502e203266ed7515190f3f580a5adb6b51fb46378bf99336669bd1731a63</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/PMC4792440/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4792440/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26978068$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Beloin, Christophe</contributor><creatorcontrib>Harris, Llinos G</creatorcontrib><creatorcontrib>Murray, Susan</creatorcontrib><creatorcontrib>Pascoe, Ben</creatorcontrib><creatorcontrib>Bray, James</creatorcontrib><creatorcontrib>Meric, Guillaume</creatorcontrib><creatorcontrib>Mageiros, Leonardos</creatorcontrib><creatorcontrib>Wilkinson, Thomas S</creatorcontrib><creatorcontrib>Jeeves, Rose</creatorcontrib><creatorcontrib>Rohde, Holger</creatorcontrib><creatorcontrib>Schwarz, Stefan</creatorcontrib><creatorcontrib>de Lencastre, Herminia</creatorcontrib><creatorcontrib>Miragaia, Maria</creatorcontrib><creatorcontrib>Rolo, Joana</creatorcontrib><creatorcontrib>Bowden, Rory</creatorcontrib><creatorcontrib>Jolley, Keith A</creatorcontrib><creatorcontrib>Maiden, Martin C J</creatorcontrib><creatorcontrib>Mack, Dietrich</creatorcontrib><creatorcontrib>Sheppard, Samuel K</creatorcontrib><title>Biofilm Morphotypes and Population Structure among Staphylococcus epidermidis from Commensal and Clinical Samples</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Bacterial species comprise related genotypes that can display divergent phenotypes with important clinical implications. Staphylococcus epidermidis is a common cause of nosocomial infections and, critical to its pathogenesis, is its ability to adhere and form biofilms on surfaces, thereby moderating the effect of the host's immune response and antibiotics. Commensal S. epidermidis populations are thought to differ from those associated with disease in factors involved in adhesion and biofilm accumulation. We quantified the differences in biofilm formation in 98 S. epidermidis isolates from various sources, and investigated population structure based on ribosomal multilocus typing (rMLST) and the presence/absence of genes involved in adhesion and biofilm formation. All isolates were able to adhere and form biofilms in in vitro growth assays and confocal microscopy allowed classification into 5 biofilm morphotypes based on their thickness, biovolume and roughness. Phylogenetic reconstruction grouped isolates into three separate clades, with the isolates in the main disease associated clade displaying diversity in morphotype. Of the biofilm morphology characteristics, only biofilm thickness had a significant association with clade distribution. The distribution of some known adhesion-associated genes (aap and sesE) among isolates showed a significant association with the species clonal frame. These data challenge the assumption that biofilm-associated genes, such as those on the ica operon, are genetic markers for less invasive S. epidermidis isolates, and suggest that phenotypic characteristics, such as adhesion and biofilm formation, are not fixed by clonal descent but are influenced by the presence of various genes that are mobile among lineages.</description><subject>Adhesion</subject><subject>Analysis</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Base sequence</subject><subject>Biofilms</subject><subject>Biofilms - classification</subject><subject>Biofilms - growth & development</subject><subject>Biology and Life Sciences</subject><subject>Confocal microscopy</subject><subject>Consortia</subject><subject>Cross Infection - microbiology</subject><subject>Epidemiology</subject><subject>Gene loci</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic markers</subject><subject>Genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotype & phenotype</subject><subject>Genotypes</subject><subject>Health aspects</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Infectious diseases</subject><subject>Laboratories</subject><subject>Life sciences</subject><subject>Medical equipment</subject><subject>Medical schools</subject><subject>Medicine and Health Sciences</subject><subject>Microscopy</subject><subject>Nosocomial infection</subject><subject>Nosocomial infections</subject><subject>Pathogenesis</subject><subject>Phylogeny</subject><subject>Physical characteristics</subject><subject>Physiological aspects</subject><subject>Population structure</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Staphylococcal Infections - microbiology</subject><subject>Staphylococcus</subject><subject>Staphylococcus aureus</subject><subject>Staphylococcus epidermidis</subject><subject>Staphylococcus epidermidis - genetics</subject><subject>Staphylococcus infections</subject><subject>Zoology</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk0uP0zAQxyMEYpeFb4AgEhKCQ4tfsZML0lLxqLRoEQWuluNMWldOnLUTRL89TptdtWgPyAe_fvMfz3gmSZ5jNMdU4HdbN_hW2XnnWpgjnGHC0IPkHBeUzDhB9OHR-ix5EsIWoYzmnD9OzggvRI54fp7cfDCuNrZJvzrfbVy_6yCkqq3Sb64brOqNa9NV7wfdDx5S1bh2Hfeq2-ys007rIaTQmQp8YyoT0tq7Jl24poE2KLsXWljTGh03K9V0FsLT5FGtbIBn03yR_Pz08cfiy-zq-vNycXk107wg_YyXeVZliEB8PuEcKpHFGAtU0zrLkcpUVfIyw3XJOBV5WRcFpZzzoqywoFhxepG8POh21gU5ZStILARlXHCSR2J5ICqntrLzplF-J50ycn_g_Foq3xttQQJkrCjzmhCFWFmRgta5ykucE1xiUULUej95G8oGKg1t75U9ET29ac1Grt1vyURBGENR4M0k4N3NAKGXjQkarFUtuGH_boY5EWSM7NU_6P3RTdRaxQBMW7voV4-i8pJllAlM0eh2fg8VRwWN0bG0YnHAqcHbE4PI9PCnX6shBLlcff9_9vrXKfv6iN2Asv0mODuMFRhOQXYAtXcheKjvkoyRHDvjNhty7Aw5dUY0e3H8QXdGt61A_wLVYwlF</recordid><startdate>20160315</startdate><enddate>20160315</enddate><creator>Harris, Llinos G</creator><creator>Murray, Susan</creator><creator>Pascoe, Ben</creator><creator>Bray, James</creator><creator>Meric, Guillaume</creator><creator>Mageiros, Leonardos</creator><creator>Wilkinson, Thomas S</creator><creator>Jeeves, Rose</creator><creator>Rohde, Holger</creator><creator>Schwarz, Stefan</creator><creator>de Lencastre, Herminia</creator><creator>Miragaia, Maria</creator><creator>Rolo, Joana</creator><creator>Bowden, Rory</creator><creator>Jolley, Keith A</creator><creator>Maiden, Martin C J</creator><creator>Mack, Dietrich</creator><creator>Sheppard, Samuel K</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>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>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160315</creationdate><title>Biofilm Morphotypes and Population Structure among Staphylococcus epidermidis from Commensal and Clinical Samples</title><author>Harris, Llinos G ; Murray, Susan ; Pascoe, Ben ; Bray, James ; Meric, Guillaume ; Mageiros, Leonardos ; Wilkinson, Thomas S ; Jeeves, Rose ; Rohde, Holger ; Schwarz, Stefan ; de Lencastre, Herminia ; Miragaia, Maria ; Rolo, Joana ; Bowden, Rory ; Jolley, Keith A ; Maiden, Martin C J ; Mack, Dietrich ; Sheppard, Samuel K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-6b85d502e203266ed7515190f3f580a5adb6b51fb46378bf99336669bd1731a63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adhesion</topic><topic>Analysis</topic><topic>Antibiotics</topic><topic>Bacteria</topic><topic>Base sequence</topic><topic>Biofilms</topic><topic>Biofilms - 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Academic</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>Harris, Llinos G</au><au>Murray, Susan</au><au>Pascoe, Ben</au><au>Bray, James</au><au>Meric, Guillaume</au><au>Mageiros, Leonardos</au><au>Wilkinson, Thomas S</au><au>Jeeves, Rose</au><au>Rohde, Holger</au><au>Schwarz, Stefan</au><au>de Lencastre, Herminia</au><au>Miragaia, Maria</au><au>Rolo, Joana</au><au>Bowden, Rory</au><au>Jolley, Keith A</au><au>Maiden, Martin C J</au><au>Mack, Dietrich</au><au>Sheppard, Samuel K</au><au>Beloin, Christophe</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Biofilm Morphotypes and Population Structure among Staphylococcus epidermidis from Commensal and Clinical Samples</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-03-15</date><risdate>2016</risdate><volume>11</volume><issue>3</issue><spage>e0151240</spage><epage>e0151240</epage><pages>e0151240-e0151240</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Bacterial species comprise related genotypes that can display divergent phenotypes with important clinical implications. Staphylococcus epidermidis is a common cause of nosocomial infections and, critical to its pathogenesis, is its ability to adhere and form biofilms on surfaces, thereby moderating the effect of the host's immune response and antibiotics. Commensal S. epidermidis populations are thought to differ from those associated with disease in factors involved in adhesion and biofilm accumulation. We quantified the differences in biofilm formation in 98 S. epidermidis isolates from various sources, and investigated population structure based on ribosomal multilocus typing (rMLST) and the presence/absence of genes involved in adhesion and biofilm formation. All isolates were able to adhere and form biofilms in in vitro growth assays and confocal microscopy allowed classification into 5 biofilm morphotypes based on their thickness, biovolume and roughness. Phylogenetic reconstruction grouped isolates into three separate clades, with the isolates in the main disease associated clade displaying diversity in morphotype. Of the biofilm morphology characteristics, only biofilm thickness had a significant association with clade distribution. The distribution of some known adhesion-associated genes (aap and sesE) among isolates showed a significant association with the species clonal frame. These data challenge the assumption that biofilm-associated genes, such as those on the ica operon, are genetic markers for less invasive S. epidermidis isolates, and suggest that phenotypic characteristics, such as adhesion and biofilm formation, are not fixed by clonal descent but are influenced by the presence of various genes that are mobile among lineages.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26978068</pmid><doi>10.1371/journal.pone.0151240</doi><oa>free_for_read</oa></addata></record> |
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identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2016-03, Vol.11 (3), p.e0151240-e0151240 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1773467628 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS) Journals Open Access; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Adhesion Analysis Antibiotics Bacteria Base sequence Biofilms Biofilms - classification Biofilms - growth & development Biology and Life Sciences Confocal microscopy Consortia Cross Infection - microbiology Epidemiology Gene loci Genes Genetic aspects Genetic markers Genetics Genomes Genomics Genotype & phenotype Genotypes Health aspects Hospitals Humans Immune response Immune system Infectious diseases Laboratories Life sciences Medical equipment Medical schools Medicine and Health Sciences Microscopy Nosocomial infection Nosocomial infections Pathogenesis Phylogeny Physical characteristics Physiological aspects Population structure Proteins Research and Analysis Methods Staphylococcal Infections - microbiology Staphylococcus Staphylococcus aureus Staphylococcus epidermidis Staphylococcus epidermidis - genetics Staphylococcus infections Zoology |
title | Biofilm Morphotypes and Population Structure among Staphylococcus epidermidis from Commensal and Clinical Samples |
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