The bacterial thiopurine methyltransferase tellurite resistance process is highly dependent upon aggregation properties and oxidative stress response
Summary Bacterial thiopurine methyltransferases (bTPMTs) can favour resistance towards toxic tellurite oxyanions through a pathway leading to the emission of a garlic‐like smell. Gene expression profiling completed by genetic, physiological and electron microscopy analyses was performed to identify...
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Veröffentlicht in: | Environmental microbiology 2012-10, Vol.14 (10), p.2645-2660 |
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creator | Prigent-Combaret, Claire Sanguin, Hervé Champier, Ludovic Bertrand, Cédric Monnez, Claire Colinon, Céline Blaha, Didier Ghigo, Jean-Marc Cournoyer, Benoit |
description | Summary
Bacterial thiopurine methyltransferases (bTPMTs) can favour resistance towards toxic tellurite oxyanions through a pathway leading to the emission of a garlic‐like smell. Gene expression profiling completed by genetic, physiological and electron microscopy analyses was performed to identify key bacterial activities contributing to this resistance process. Escherichia coli strain MG1655 expressing the bTPMT was used as a cell model in these experiments. This strain produced a garlic‐like smell which was found to be due to dimethyl telluride, and cell aggregates in culture media supplemented with tellurite. Properties involved in aggregation were correlated with cell attachment to polystyrene, which increased with tellurite concentrations. Gene expression profiling supported a role of adhesins in the resistance process with 14% of the tellurite‐regulated genes involved in cell envelope, flagella and fimbriae biogenesis. Other tellurite‐regulated genes were, at 27%, involved in energy, carbohydrate and amino acid metabolism including the synthesis of antioxidant proteins, and at 12% in the synthesis of transcriptional regulators and signal transduction systems. Escherichia coli mutants impaired in tellurite‐regulated genes showed ubiquinone and adhesins synthesis, oxidative stress response, and efflux to be essential in the bTPMT resistance process. High tellurite resistance required a synergistic expression of these functions and an efficient tellurium volatilization by the bTPMT. |
doi_str_mv | 10.1111/j.1462-2920.2012.02802.x |
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Bacterial thiopurine methyltransferases (bTPMTs) can favour resistance towards toxic tellurite oxyanions through a pathway leading to the emission of a garlic‐like smell. Gene expression profiling completed by genetic, physiological and electron microscopy analyses was performed to identify key bacterial activities contributing to this resistance process. Escherichia coli strain MG1655 expressing the bTPMT was used as a cell model in these experiments. This strain produced a garlic‐like smell which was found to be due to dimethyl telluride, and cell aggregates in culture media supplemented with tellurite. Properties involved in aggregation were correlated with cell attachment to polystyrene, which increased with tellurite concentrations. Gene expression profiling supported a role of adhesins in the resistance process with 14% of the tellurite‐regulated genes involved in cell envelope, flagella and fimbriae biogenesis. Other tellurite‐regulated genes were, at 27%, involved in energy, carbohydrate and amino acid metabolism including the synthesis of antioxidant proteins, and at 12% in the synthesis of transcriptional regulators and signal transduction systems. Escherichia coli mutants impaired in tellurite‐regulated genes showed ubiquinone and adhesins synthesis, oxidative stress response, and efflux to be essential in the bTPMT resistance process. High tellurite resistance required a synergistic expression of these functions and an efficient tellurium volatilization by the bTPMT.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/j.1462-2920.2012.02802.x</identifier><identifier>PMID: 22708879</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Adhesins, Bacterial - metabolism ; Drug Resistance, Bacterial - physiology ; Enzyme Inhibitors - pharmacology ; Escherichia coli ; Escherichia coli - drug effects ; Escherichia coli - enzymology ; Escherichia coli - genetics ; Escherichia coli - growth & development ; Escherichia coli - ultrastructure ; Gene Expression Profiling ; Gene Expression Regulation, Bacterial ; Gene Knockout Techniques ; Genes, Bacterial - genetics ; Life Sciences ; Methylation ; Methyltransferases - metabolism ; Microbiology and Parasitology ; Mutation ; Oxidation-Reduction ; Oxidative Stress ; Tellurium - metabolism ; Tellurium - pharmacology</subject><ispartof>Environmental microbiology, 2012-10, Vol.14 (10), p.2645-2660</ispartof><rights>2012 Society for Applied Microbiology and Blackwell Publishing Ltd</rights><rights>2012 Society for Applied Microbiology and Blackwell Publishing Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5402-7e46aeef81b5da858794416ccabe2abbb3e9fb9ef8c6336d909ad4e433e48e643</citedby><cites>FETCH-LOGICAL-c5402-7e46aeef81b5da858794416ccabe2abbb3e9fb9ef8c6336d909ad4e433e48e643</cites><orcidid>0000-0001-8968-0660</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1462-2920.2012.02802.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1462-2920.2012.02802.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,777,781,882,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22708879$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://univ-lyon1.hal.science/hal-02532812$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Prigent-Combaret, Claire</creatorcontrib><creatorcontrib>Sanguin, Hervé</creatorcontrib><creatorcontrib>Champier, Ludovic</creatorcontrib><creatorcontrib>Bertrand, Cédric</creatorcontrib><creatorcontrib>Monnez, Claire</creatorcontrib><creatorcontrib>Colinon, Céline</creatorcontrib><creatorcontrib>Blaha, Didier</creatorcontrib><creatorcontrib>Ghigo, Jean-Marc</creatorcontrib><creatorcontrib>Cournoyer, Benoit</creatorcontrib><title>The bacterial thiopurine methyltransferase tellurite resistance process is highly dependent upon aggregation properties and oxidative stress response</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Bacterial thiopurine methyltransferases (bTPMTs) can favour resistance towards toxic tellurite oxyanions through a pathway leading to the emission of a garlic‐like smell. Gene expression profiling completed by genetic, physiological and electron microscopy analyses was performed to identify key bacterial activities contributing to this resistance process. Escherichia coli strain MG1655 expressing the bTPMT was used as a cell model in these experiments. This strain produced a garlic‐like smell which was found to be due to dimethyl telluride, and cell aggregates in culture media supplemented with tellurite. Properties involved in aggregation were correlated with cell attachment to polystyrene, which increased with tellurite concentrations. Gene expression profiling supported a role of adhesins in the resistance process with 14% of the tellurite‐regulated genes involved in cell envelope, flagella and fimbriae biogenesis. Other tellurite‐regulated genes were, at 27%, involved in energy, carbohydrate and amino acid metabolism including the synthesis of antioxidant proteins, and at 12% in the synthesis of transcriptional regulators and signal transduction systems. Escherichia coli mutants impaired in tellurite‐regulated genes showed ubiquinone and adhesins synthesis, oxidative stress response, and efflux to be essential in the bTPMT resistance process. High tellurite resistance required a synergistic expression of these functions and an efficient tellurium volatilization by the bTPMT.</description><subject>Adhesins, Bacterial - metabolism</subject><subject>Drug Resistance, Bacterial - physiology</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Escherichia coli</subject><subject>Escherichia coli - drug effects</subject><subject>Escherichia coli - enzymology</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - growth & development</subject><subject>Escherichia coli - ultrastructure</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gene Knockout Techniques</subject><subject>Genes, Bacterial - genetics</subject><subject>Life Sciences</subject><subject>Methylation</subject><subject>Methyltransferases - metabolism</subject><subject>Microbiology and Parasitology</subject><subject>Mutation</subject><subject>Oxidation-Reduction</subject><subject>Oxidative Stress</subject><subject>Tellurium - metabolism</subject><subject>Tellurium - pharmacology</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNksuO1DAQRSMEYh7wC8hLWCT4lcRZsBiN5iU1sKARS6uSVDpu0kmwnaH7Q_jfcciQNV7YJde517Kvo4gwmrAwPu4TJjMe84LThFPGE8oV5cnxRXS-Nl6uNeNn0YVze0pZLnL6OjrjPKdK5cV59GfbIimh8mgNdMS3Zhgna3okB_TtqfMWetegBYfEY9eFnkdi0Rnnoa-QjHao0DliHGnNru1OpMYR-xp7T6Zx6AnsdhZ34E2oAzyi9QYdgb4mw9HUofGIxHk7m4QpSBy-iV410Dl8-7xeRt9vb7bX9_Hm693D9dUmrlJJeZyjzACxUaxMa1BpuJGULKsqKJFDWZYCi6YsAlBlQmR1QQuoJUohUCrMpLiMPiy-LXR6tOYA9qQHMPr-aqPnPcpTwRXjjyyw7xc2XOLXhM7rg3FVeBLocZicZoynXBR5WgRULWhlB-csNqs3o3oOUO_1nI2ec9JzgPpvgPoYpO-eT5nKA9ar8F9iAfi0AL9Nh6f_NtY3nx_mKujjRR8CxOOqB_tTZ-F3pPrHlztdbLbbb7nKtBJPrgW9Zw</recordid><startdate>201210</startdate><enddate>201210</enddate><creator>Prigent-Combaret, Claire</creator><creator>Sanguin, Hervé</creator><creator>Champier, Ludovic</creator><creator>Bertrand, Cédric</creator><creator>Monnez, Claire</creator><creator>Colinon, Céline</creator><creator>Blaha, Didier</creator><creator>Ghigo, Jean-Marc</creator><creator>Cournoyer, Benoit</creator><general>Blackwell Publishing Ltd</general><general>Society for Applied Microbiology and Wiley-Blackwell</general><scope>BSCLL</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>7QL</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-8968-0660</orcidid></search><sort><creationdate>201210</creationdate><title>The bacterial thiopurine methyltransferase tellurite resistance process is highly dependent upon aggregation properties and oxidative stress response</title><author>Prigent-Combaret, Claire ; Sanguin, Hervé ; Champier, Ludovic ; Bertrand, Cédric ; Monnez, Claire ; Colinon, Céline ; Blaha, Didier ; Ghigo, Jean-Marc ; Cournoyer, Benoit</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5402-7e46aeef81b5da858794416ccabe2abbb3e9fb9ef8c6336d909ad4e433e48e643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Adhesins, Bacterial - metabolism</topic><topic>Drug Resistance, Bacterial - physiology</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>Escherichia coli</topic><topic>Escherichia coli - drug effects</topic><topic>Escherichia coli - enzymology</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - growth & development</topic><topic>Escherichia coli - ultrastructure</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Gene Knockout Techniques</topic><topic>Genes, Bacterial - genetics</topic><topic>Life Sciences</topic><topic>Methylation</topic><topic>Methyltransferases - metabolism</topic><topic>Microbiology and Parasitology</topic><topic>Mutation</topic><topic>Oxidation-Reduction</topic><topic>Oxidative Stress</topic><topic>Tellurium - metabolism</topic><topic>Tellurium - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Prigent-Combaret, Claire</creatorcontrib><creatorcontrib>Sanguin, Hervé</creatorcontrib><creatorcontrib>Champier, Ludovic</creatorcontrib><creatorcontrib>Bertrand, Cédric</creatorcontrib><creatorcontrib>Monnez, Claire</creatorcontrib><creatorcontrib>Colinon, Céline</creatorcontrib><creatorcontrib>Blaha, Didier</creatorcontrib><creatorcontrib>Ghigo, Jean-Marc</creatorcontrib><creatorcontrib>Cournoyer, Benoit</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Prigent-Combaret, Claire</au><au>Sanguin, Hervé</au><au>Champier, Ludovic</au><au>Bertrand, Cédric</au><au>Monnez, Claire</au><au>Colinon, Céline</au><au>Blaha, Didier</au><au>Ghigo, Jean-Marc</au><au>Cournoyer, Benoit</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The bacterial thiopurine methyltransferase tellurite resistance process is highly dependent upon aggregation properties and oxidative stress response</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2012-10</date><risdate>2012</risdate><volume>14</volume><issue>10</issue><spage>2645</spage><epage>2660</epage><pages>2645-2660</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Bacterial thiopurine methyltransferases (bTPMTs) can favour resistance towards toxic tellurite oxyanions through a pathway leading to the emission of a garlic‐like smell. Gene expression profiling completed by genetic, physiological and electron microscopy analyses was performed to identify key bacterial activities contributing to this resistance process. Escherichia coli strain MG1655 expressing the bTPMT was used as a cell model in these experiments. This strain produced a garlic‐like smell which was found to be due to dimethyl telluride, and cell aggregates in culture media supplemented with tellurite. Properties involved in aggregation were correlated with cell attachment to polystyrene, which increased with tellurite concentrations. Gene expression profiling supported a role of adhesins in the resistance process with 14% of the tellurite‐regulated genes involved in cell envelope, flagella and fimbriae biogenesis. Other tellurite‐regulated genes were, at 27%, involved in energy, carbohydrate and amino acid metabolism including the synthesis of antioxidant proteins, and at 12% in the synthesis of transcriptional regulators and signal transduction systems. Escherichia coli mutants impaired in tellurite‐regulated genes showed ubiquinone and adhesins synthesis, oxidative stress response, and efflux to be essential in the bTPMT resistance process. High tellurite resistance required a synergistic expression of these functions and an efficient tellurium volatilization by the bTPMT.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>22708879</pmid><doi>10.1111/j.1462-2920.2012.02802.x</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-8968-0660</orcidid></addata></record> |
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subjects | Adhesins, Bacterial - metabolism Drug Resistance, Bacterial - physiology Enzyme Inhibitors - pharmacology Escherichia coli Escherichia coli - drug effects Escherichia coli - enzymology Escherichia coli - genetics Escherichia coli - growth & development Escherichia coli - ultrastructure Gene Expression Profiling Gene Expression Regulation, Bacterial Gene Knockout Techniques Genes, Bacterial - genetics Life Sciences Methylation Methyltransferases - metabolism Microbiology and Parasitology Mutation Oxidation-Reduction Oxidative Stress Tellurium - metabolism Tellurium - pharmacology |
title | The bacterial thiopurine methyltransferase tellurite resistance process is highly dependent upon aggregation properties and oxidative stress response |
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