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Environmentally co‐occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context‐dependent fitness effects
Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co‐occurring pQBR family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluor...
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Published in: | Environmental microbiology 2015-12, Vol.17 (12), p.5008-5022 |
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creator | Hall, James P.J Harrison, Ellie Lilley, Andrew K Paterson, Steve Spiers, Andrew J Brockhurst, Michael A |
description | Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co‐occurring pQBR family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid‐borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus‐encoding cluster and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolize sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity among co‐occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity. |
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We compared the sequences of four co‐occurring pQBR family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid‐borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus‐encoding cluster and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolize sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity among co‐occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.12901</identifier><identifier>PMID: 25969927</identifier><language>eng</language><publisher>England: Blackwell Science</publisher><subject>arylsulfatase ; Arylsulfatases - genetics ; Bacteriology ; chemotaxis ; DNA Transposable Elements - genetics ; Drug Resistance, Bacterial - genetics ; Environment ; evolution ; Gene Transfer, Horizontal ; horizontal gene transfer ; mercury ; Mercury - pharmacology ; microbial communities ; operon ; Operon - genetics ; phenotypic variation ; Plasmids ; Plasmids - genetics ; Pseudomonas ; Pseudomonas fluorescens ; Pseudomonas fluorescens - drug effects ; Pseudomonas fluorescens - genetics ; Pseudomonas fluorescens - isolation & purification ; Soil Microbiology ; sucrose ; Sucrose - metabolism ; transposons</subject><ispartof>Environmental microbiology, 2015-12, Vol.17 (12), p.5008-5022</ispartof><rights>2015 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2015 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6321-7d13a695452a9d1d4549a16e87b4841cd8a4099f727931781584db1190fd0173</citedby><cites>FETCH-LOGICAL-c6321-7d13a695452a9d1d4549a16e87b4841cd8a4099f727931781584db1190fd0173</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25969927$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hall, James P.J</creatorcontrib><creatorcontrib>Harrison, Ellie</creatorcontrib><creatorcontrib>Lilley, Andrew K</creatorcontrib><creatorcontrib>Paterson, Steve</creatorcontrib><creatorcontrib>Spiers, Andrew J</creatorcontrib><creatorcontrib>Brockhurst, Michael A</creatorcontrib><title>Environmentally co‐occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context‐dependent fitness effects</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co‐occurring pQBR family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid‐borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus‐encoding cluster and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolize sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity among co‐occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.</description><subject>arylsulfatase</subject><subject>Arylsulfatases - genetics</subject><subject>Bacteriology</subject><subject>chemotaxis</subject><subject>DNA Transposable Elements - genetics</subject><subject>Drug Resistance, Bacterial - genetics</subject><subject>Environment</subject><subject>evolution</subject><subject>Gene Transfer, Horizontal</subject><subject>horizontal gene transfer</subject><subject>mercury</subject><subject>Mercury - pharmacology</subject><subject>microbial communities</subject><subject>operon</subject><subject>Operon - genetics</subject><subject>phenotypic variation</subject><subject>Plasmids</subject><subject>Plasmids - genetics</subject><subject>Pseudomonas</subject><subject>Pseudomonas fluorescens</subject><subject>Pseudomonas fluorescens - drug effects</subject><subject>Pseudomonas fluorescens - genetics</subject><subject>Pseudomonas fluorescens - isolation & purification</subject><subject>Soil Microbiology</subject><subject>sucrose</subject><subject>Sucrose - metabolism</subject><subject>transposons</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNqFkstu1DAUhiMEohdYs4NIbNgMtR07jjdIpRqGSqUgUYTUjeWxT6YuiR3sZNrZ8Qi8AC_Hk-C5NAI29caX853fx8d_lj3D6DVO4wjTkkyIIGlLBMIPsv3x5OG4xmQvO4jxGiHMC44eZ3uEiVIIwvezX1O3tMG7FlyvmmaVa__7x0-v9RCCdYu8hZCWqzxAtLFXTkPeNSq21sRcBcgX4KC3epOqnMm7K3C-X3W7I2OXECJsQtq7GkK-VMGqeQPrfQ-3fbrOQAfOpAry2vYOYsyhrkH38Un2qFZNhKe7-TC7eDe9OHk_Ofs4Oz05PpvosiB4wg0uVCkYZUQJgw1lVChcQsXntKJYm0pRJETNCRcF5hVmFTVzjAWqzbonh9mbrWw3zFswOlUSVCO7YFsVVtIrK_-NOHslF34pqagEZUUSeLUTCP77ALGXrY0amkY58EOUWGAhSlqi6n6Ulyj9DOIsoS__Q6_9EFxqRKIYJ4hwihN1tKV08DEGqMe6MZJrk8i1DeTaEnJjkpTx_O_njvydKxLAtsCNbWB1n56cfji9E55s85JV4HbMU-GbLJPzmPx6PpOfLs_J7BIX8m3iX2z5WnmpFsFG-eUzQbhMTiWMVaL4A4PF5C8</recordid><startdate>201512</startdate><enddate>201512</enddate><creator>Hall, James P.J</creator><creator>Harrison, Ellie</creator><creator>Lilley, Andrew K</creator><creator>Paterson, Steve</creator><creator>Spiers, Andrew J</creator><creator>Brockhurst, Michael A</creator><general>Blackwell Science</general><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>FBQ</scope><scope>BSCLL</scope><scope>24P</scope><scope>WIN</scope><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>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>201512</creationdate><title>Environmentally co‐occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context‐dependent fitness effects</title><author>Hall, James P.J ; Harrison, Ellie ; Lilley, Andrew K ; Paterson, Steve ; Spiers, Andrew J ; Brockhurst, Michael A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6321-7d13a695452a9d1d4549a16e87b4841cd8a4099f727931781584db1190fd0173</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>arylsulfatase</topic><topic>Arylsulfatases - genetics</topic><topic>Bacteriology</topic><topic>chemotaxis</topic><topic>DNA Transposable Elements - genetics</topic><topic>Drug Resistance, Bacterial - genetics</topic><topic>Environment</topic><topic>evolution</topic><topic>Gene Transfer, Horizontal</topic><topic>horizontal gene transfer</topic><topic>mercury</topic><topic>Mercury - pharmacology</topic><topic>microbial communities</topic><topic>operon</topic><topic>Operon - genetics</topic><topic>phenotypic variation</topic><topic>Plasmids</topic><topic>Plasmids - genetics</topic><topic>Pseudomonas</topic><topic>Pseudomonas fluorescens</topic><topic>Pseudomonas fluorescens - drug effects</topic><topic>Pseudomonas fluorescens - genetics</topic><topic>Pseudomonas fluorescens - isolation & purification</topic><topic>Soil Microbiology</topic><topic>sucrose</topic><topic>Sucrose - metabolism</topic><topic>transposons</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hall, James P.J</creatorcontrib><creatorcontrib>Harrison, Ellie</creatorcontrib><creatorcontrib>Lilley, Andrew K</creatorcontrib><creatorcontrib>Paterson, Steve</creatorcontrib><creatorcontrib>Spiers, Andrew J</creatorcontrib><creatorcontrib>Brockhurst, Michael A</creatorcontrib><collection>AGRIS</collection><collection>Istex</collection><collection>Wiley Open Access</collection><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hall, James P.J</au><au>Harrison, Ellie</au><au>Lilley, Andrew K</au><au>Paterson, Steve</au><au>Spiers, Andrew J</au><au>Brockhurst, Michael A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Environmentally co‐occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context‐dependent fitness effects</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2015-12</date><risdate>2015</risdate><volume>17</volume><issue>12</issue><spage>5008</spage><epage>5022</epage><pages>5008-5022</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co‐occurring pQBR family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid‐borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus‐encoding cluster and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolize sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity among co‐occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.</abstract><cop>England</cop><pub>Blackwell Science</pub><pmid>25969927</pmid><doi>10.1111/1462-2920.12901</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | arylsulfatase Arylsulfatases - genetics Bacteriology chemotaxis DNA Transposable Elements - genetics Drug Resistance, Bacterial - genetics Environment evolution Gene Transfer, Horizontal horizontal gene transfer mercury Mercury - pharmacology microbial communities operon Operon - genetics phenotypic variation Plasmids Plasmids - genetics Pseudomonas Pseudomonas fluorescens Pseudomonas fluorescens - drug effects Pseudomonas fluorescens - genetics Pseudomonas fluorescens - isolation & purification Soil Microbiology sucrose Sucrose - metabolism transposons |
title | Environmentally co‐occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context‐dependent fitness effects |
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