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Extracellular DNA release from the genome-reduced pathogen Mycoplasma hyopneumoniae is essential for biofilm formation on abiotic surfaces
Mycoplasma hyopneumoniae is an economically devastating, globally disseminated pathogen that can maintain a chronic infectious state within its host, swine. Here, we depict the events underpinning M . hyopneumoniae biofilm formation on an abiotic surface and demonstrate for the first time, biofilms...
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Published in: | Scientific reports 2018-07, Vol.8 (1), p.10373-12, Article 10373 |
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description | Mycoplasma hyopneumoniae
is an economically devastating, globally disseminated pathogen that can maintain a chronic infectious state within its host, swine. Here, we depict the events underpinning
M
.
hyopneumoniae
biofilm formation on an abiotic surface and demonstrate for the first time, biofilms forming on porcine epithelial cell monolayers and in the lungs of pigs, experimentally infected with
M
.
hyopneumoniae
. Nuclease treatment prevents biofilms forming on glass but not on porcine epithelial cells indicating that extracellular DNA (eDNA), which localises at the base of biofilms, is critical in the formation of these structures on abiotic surfaces. Subpopulations of
M
.
hyopneumoniae
cells, denoted by their ability to take up the dye TOTO-1 and release eDNA, were identified. A visually distinct sub-population of pleomorphic cells, that we refer to here as large cell variants (LCVs), rapidly transition from phase dark to translucent “ghost” cells. The translucent cells accumulate the membrane-impermeable dye TOTO-1, forming readily discernible membrane breaches immediately prior to lysis and the possible release of eDNA and other intracellular content (public goods) into the extracellular environment. Our novel observations expand knowledge of the lifestyles adopted by this wall-less, genome-reduced pathogen and provide further insights to its survival within farm environments and swine. |
doi_str_mv | 10.1038/s41598-018-28678-2 |
format | article |
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is an economically devastating, globally disseminated pathogen that can maintain a chronic infectious state within its host, swine. Here, we depict the events underpinning
M
.
hyopneumoniae
biofilm formation on an abiotic surface and demonstrate for the first time, biofilms forming on porcine epithelial cell monolayers and in the lungs of pigs, experimentally infected with
M
.
hyopneumoniae
. Nuclease treatment prevents biofilms forming on glass but not on porcine epithelial cells indicating that extracellular DNA (eDNA), which localises at the base of biofilms, is critical in the formation of these structures on abiotic surfaces. Subpopulations of
M
.
hyopneumoniae
cells, denoted by their ability to take up the dye TOTO-1 and release eDNA, were identified. A visually distinct sub-population of pleomorphic cells, that we refer to here as large cell variants (LCVs), rapidly transition from phase dark to translucent “ghost” cells. The translucent cells accumulate the membrane-impermeable dye TOTO-1, forming readily discernible membrane breaches immediately prior to lysis and the possible release of eDNA and other intracellular content (public goods) into the extracellular environment. Our novel observations expand knowledge of the lifestyles adopted by this wall-less, genome-reduced pathogen and provide further insights to its survival within farm environments and swine.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-018-28678-2</identifier><identifier>PMID: 29991767</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14 ; 14/1 ; 14/19 ; 14/28 ; 14/63 ; 631/326/421 ; 631/326/46 ; 82/51 ; Biofilms ; Deoxyribonucleic acid ; DNA ; Dyes ; Environmental DNA ; Epithelial cells ; Genomes ; Humanities and Social Sciences ; Lysis ; multidisciplinary ; Mycoplasma hyopneumoniae ; Nuclease ; Pathogens ; Science ; Science (multidisciplinary) ; Subpopulations ; Swine</subject><ispartof>Scientific reports, 2018-07, Vol.8 (1), p.10373-12, Article 10373</ispartof><rights>The Author(s) 2018</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c478t-c3f55c3cc890e8b27c8ec5b2b49b440d1c86ab8d8c60c373c7203ab9cb4867353</citedby><cites>FETCH-LOGICAL-c478t-c3f55c3cc890e8b27c8ec5b2b49b440d1c86ab8d8c60c373c7203ab9cb4867353</cites><orcidid>0000-0003-2296-3791</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2068311033/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2068311033?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,44566,53766,53768,74869</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29991767$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Raymond, Benjamin B. A.</creatorcontrib><creatorcontrib>Jenkins, Cheryl</creatorcontrib><creatorcontrib>Turnbull, Lynne</creatorcontrib><creatorcontrib>Whitchurch, Cynthia B.</creatorcontrib><creatorcontrib>Djordjevic, Steven P.</creatorcontrib><title>Extracellular DNA release from the genome-reduced pathogen Mycoplasma hyopneumoniae is essential for biofilm formation on abiotic surfaces</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Mycoplasma hyopneumoniae
is an economically devastating, globally disseminated pathogen that can maintain a chronic infectious state within its host, swine. Here, we depict the events underpinning
M
.
hyopneumoniae
biofilm formation on an abiotic surface and demonstrate for the first time, biofilms forming on porcine epithelial cell monolayers and in the lungs of pigs, experimentally infected with
M
.
hyopneumoniae
. Nuclease treatment prevents biofilms forming on glass but not on porcine epithelial cells indicating that extracellular DNA (eDNA), which localises at the base of biofilms, is critical in the formation of these structures on abiotic surfaces. Subpopulations of
M
.
hyopneumoniae
cells, denoted by their ability to take up the dye TOTO-1 and release eDNA, were identified. A visually distinct sub-population of pleomorphic cells, that we refer to here as large cell variants (LCVs), rapidly transition from phase dark to translucent “ghost” cells. The translucent cells accumulate the membrane-impermeable dye TOTO-1, forming readily discernible membrane breaches immediately prior to lysis and the possible release of eDNA and other intracellular content (public goods) into the extracellular environment. Our novel observations expand knowledge of the lifestyles adopted by this wall-less, genome-reduced pathogen and provide further insights to its survival within farm environments and swine.</description><subject>14</subject><subject>14/1</subject><subject>14/19</subject><subject>14/28</subject><subject>14/63</subject><subject>631/326/421</subject><subject>631/326/46</subject><subject>82/51</subject><subject>Biofilms</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Dyes</subject><subject>Environmental DNA</subject><subject>Epithelial cells</subject><subject>Genomes</subject><subject>Humanities and Social Sciences</subject><subject>Lysis</subject><subject>multidisciplinary</subject><subject>Mycoplasma hyopneumoniae</subject><subject>Nuclease</subject><subject>Pathogens</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Subpopulations</subject><subject>Swine</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNp9Uctu1TAQtRAVrdr-AAtkiXXAryT2BqkqpSAVuilry5lM7nXlxMFOKu4v8NV1uaWUDZblGc2cOXPkQ8hrzt5xJvX7rHhtdMW4roRu2vK-IEeCqboSUoiXz_JDcprzLSunFkZx84ocCmMMb5v2iPy6-LkkBxjCGlyiH7-d0YQBXUY6pDjSZYt0g1McsUrYr4A9nd2yjaVGv-4gzsHl0dHtLs4TrmOcvEPqM8WccVq8C3SIiXY-Dj6MD_noFh8nWq4r1cUDzWsaioJ8Qg4GFzKePsZj8v3Txc355-rq-vLL-dlVBarVSwVyqGuQANow1J1oQSPUneiU6ZRiPQfduE73GhoGspXQCiZdZ6BT5Z9kLY_Jhz3vvHYj9lB0JhfsnPzo0s5G5-2_nclv7Sbe2YZJo1pVCN4-EqT4Y8W82Nu4pqlotoI1WvJikCwosUdBijknHJ42cGYfLLR7C22x0P620Ioy9Oa5tqeRP4YVgNwDcmlNG0x_d_-H9h5kqKtG</recordid><startdate>20180710</startdate><enddate>20180710</enddate><creator>Raymond, Benjamin B. A.</creator><creator>Jenkins, Cheryl</creator><creator>Turnbull, Lynne</creator><creator>Whitchurch, Cynthia B.</creator><creator>Djordjevic, Steven P.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2296-3791</orcidid></search><sort><creationdate>20180710</creationdate><title>Extracellular DNA release from the genome-reduced pathogen Mycoplasma hyopneumoniae is essential for biofilm formation on abiotic surfaces</title><author>Raymond, Benjamin B. A. ; Jenkins, Cheryl ; Turnbull, Lynne ; Whitchurch, Cynthia B. ; Djordjevic, Steven P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c478t-c3f55c3cc890e8b27c8ec5b2b49b440d1c86ab8d8c60c373c7203ab9cb4867353</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>14</topic><topic>14/1</topic><topic>14/19</topic><topic>14/28</topic><topic>14/63</topic><topic>631/326/421</topic><topic>631/326/46</topic><topic>82/51</topic><topic>Biofilms</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Dyes</topic><topic>Environmental DNA</topic><topic>Epithelial cells</topic><topic>Genomes</topic><topic>Humanities and Social Sciences</topic><topic>Lysis</topic><topic>multidisciplinary</topic><topic>Mycoplasma hyopneumoniae</topic><topic>Nuclease</topic><topic>Pathogens</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Subpopulations</topic><topic>Swine</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Raymond, Benjamin B. A.</creatorcontrib><creatorcontrib>Jenkins, Cheryl</creatorcontrib><creatorcontrib>Turnbull, Lynne</creatorcontrib><creatorcontrib>Whitchurch, Cynthia B.</creatorcontrib><creatorcontrib>Djordjevic, Steven P.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Science Database (ProQuest)</collection><collection>ProQuest Biological Science Journals</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Raymond, Benjamin B. A.</au><au>Jenkins, Cheryl</au><au>Turnbull, Lynne</au><au>Whitchurch, Cynthia B.</au><au>Djordjevic, Steven P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Extracellular DNA release from the genome-reduced pathogen Mycoplasma hyopneumoniae is essential for biofilm formation on abiotic surfaces</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2018-07-10</date><risdate>2018</risdate><volume>8</volume><issue>1</issue><spage>10373</spage><epage>12</epage><pages>10373-12</pages><artnum>10373</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Mycoplasma hyopneumoniae
is an economically devastating, globally disseminated pathogen that can maintain a chronic infectious state within its host, swine. Here, we depict the events underpinning
M
.
hyopneumoniae
biofilm formation on an abiotic surface and demonstrate for the first time, biofilms forming on porcine epithelial cell monolayers and in the lungs of pigs, experimentally infected with
M
.
hyopneumoniae
. Nuclease treatment prevents biofilms forming on glass but not on porcine epithelial cells indicating that extracellular DNA (eDNA), which localises at the base of biofilms, is critical in the formation of these structures on abiotic surfaces. Subpopulations of
M
.
hyopneumoniae
cells, denoted by their ability to take up the dye TOTO-1 and release eDNA, were identified. A visually distinct sub-population of pleomorphic cells, that we refer to here as large cell variants (LCVs), rapidly transition from phase dark to translucent “ghost” cells. The translucent cells accumulate the membrane-impermeable dye TOTO-1, forming readily discernible membrane breaches immediately prior to lysis and the possible release of eDNA and other intracellular content (public goods) into the extracellular environment. Our novel observations expand knowledge of the lifestyles adopted by this wall-less, genome-reduced pathogen and provide further insights to its survival within farm environments and swine.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>29991767</pmid><doi>10.1038/s41598-018-28678-2</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-2296-3791</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 14 14/1 14/19 14/28 14/63 631/326/421 631/326/46 82/51 Biofilms Deoxyribonucleic acid DNA Dyes Environmental DNA Epithelial cells Genomes Humanities and Social Sciences Lysis multidisciplinary Mycoplasma hyopneumoniae Nuclease Pathogens Science Science (multidisciplinary) Subpopulations Swine |
title | Extracellular DNA release from the genome-reduced pathogen Mycoplasma hyopneumoniae is essential for biofilm formation on abiotic surfaces |
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