Ectoine and Hydroxyectoine as Protectants against Osmotic and Cold Stress: Uptake through the SigB-Controlled Betaine-Choline- Carnitine Transporter-Type Carrier EctT from Virgibacillus pantothenticus
Virgibacillus pantothenticus has been shown to synthesize the compatible solute ectoine in response to high salinity or low growth temperature. We found that exogenously provided ectoine and hydroxyectoine also serve as protectants against these challenges. Transport studies with [14C]ectoine reveal...
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| Veröffentlicht in: | Journal of Bacteriology 2011-09, Vol.193 (18), p.4699-4708 |
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| creator | Kuhlmann, Anne U Hoffmann, Tamara Bursy, Jan Jebbar, Mohamed Bremer, Erhard |
| description | Virgibacillus pantothenticus has been shown to synthesize the compatible solute ectoine in response to high salinity or low growth temperature. We found that exogenously provided ectoine and hydroxyectoine also serve as protectants against these challenges. Transport studies with [14C]ectoine revealed that both types of stress induced a high-affinity ectoine uptake activity in V. pantothenticus. By using an Escherichia coli mutant defective in osmoprotectant uptake systems, a functional complementation approach for osmostress resistance in the presence of ectoine was employed to retrieve a gene encoding an ectoine transporter from V. pantothenticus. The cloned gene (ectT) encodes a protein (EctT) that is a member of the BCCT (betaine-choline-carnitine-transporter) family of carriers. Osmoprotection assays demonstrated that the EctT carrier mediates the preferential import of ectoine and hydroxyectoine but also possesses minor uptake activities for the compatible solutes proline and glycine betaine. Northern blot analysis with RNA isolated from V. pantothenticus revealed that a rise in the external osmolality or a reduction in growth temperature strongly increased the transcription of the ectT gene. Primer extension analysis demonstrated that ectT was transcribed under these conditions from a SigB-type promoter. SigB is the master regulator of the general stress regulon of bacilli and provides protection to cells against various challenges, including high salinity and low temperature. Both the synthesis of ectoine and the EctT-mediated uptake of ectoine and hydroxyectoine are triggered by the same environmental cues, high salinity and cold stress, and thereby provide, in a concerted fashion, the protection of V. pantothenticus against these challenges. |
| doi_str_mv | 10.1128/JB.05270-11 |
| format | Article |
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We found that exogenously provided ectoine and hydroxyectoine also serve as protectants against these challenges. Transport studies with [14C]ectoine revealed that both types of stress induced a high-affinity ectoine uptake activity in V. pantothenticus. By using an Escherichia coli mutant defective in osmoprotectant uptake systems, a functional complementation approach for osmostress resistance in the presence of ectoine was employed to retrieve a gene encoding an ectoine transporter from V. pantothenticus. The cloned gene (ectT) encodes a protein (EctT) that is a member of the BCCT (betaine-choline-carnitine-transporter) family of carriers. Osmoprotection assays demonstrated that the EctT carrier mediates the preferential import of ectoine and hydroxyectoine but also possesses minor uptake activities for the compatible solutes proline and glycine betaine. Northern blot analysis with RNA isolated from V. pantothenticus revealed that a rise in the external osmolality or a reduction in growth temperature strongly increased the transcription of the ectT gene. Primer extension analysis demonstrated that ectT was transcribed under these conditions from a SigB-type promoter. SigB is the master regulator of the general stress regulon of bacilli and provides protection to cells against various challenges, including high salinity and low temperature. Both the synthesis of ectoine and the EctT-mediated uptake of ectoine and hydroxyectoine are triggered by the same environmental cues, high salinity and cold stress, and thereby provide, in a concerted fashion, the protection of V. pantothenticus against these challenges.</description><identifier>ISSN: 0021-9193</identifier><identifier>EISSN: 1098-5530</identifier><identifier>EISSN: 1067-8832</identifier><identifier>DOI: 10.1128/JB.05270-11</identifier><identifier>PMID: 21764932</identifier><identifier>CODEN: JOBAAY</identifier><language>eng</language><publisher>Washington, DC: American Society for Microbiology</publisher><subject>Abiotic stress ; Amino Acids, Diamino ; Amino Acids, Diamino - metabolism ; Bacterial Proteins ; Bacterial Proteins - metabolism ; Bacteriology ; betaine ; Biological and medical sciences ; Blotting, Northern ; Carbon Radioisotopes ; Carbon Radioisotopes - metabolism ; carnitine ; Chemical compounds ; chemistry ; Cloning ; cold stress ; cold tolerance ; Cold-Shock Response ; DNA, Bacterial ; DNA, Bacterial - chemistry ; DNA, Bacterial - genetics ; Drug resistance ; E coli ; Escherichia coli ; Escherichia coli - genetics ; Escherichia coli - metabolism ; Fundamental and applied biological sciences. Psychology ; Gene Expression Profiling ; Gene Expression Regulation, Bacterial ; Genetic Complementation Test ; genetics ; growth retardation ; Membrane Transport Proteins ; Membrane Transport Proteins - genetics ; Membrane Transport Proteins - metabolism ; metabolism ; methods ; Microbiology ; Miscellaneous ; Molecular Sequence Data ; mutants ; Mutation ; Northern blotting ; osmolality ; Osmotic Pressure ; osmotic stress ; osmotolerance ; physiology ; Physiology and Metabolism ; proline ; regulon ; RNA ; salinity ; Sequence Analysis, DNA ; Sigma Factor ; Sigma Factor - metabolism ; solutes ; Staining and Labeling ; Staining and Labeling - methods ; Stress, Physiological ; Substrate Specificity ; temperature ; Transcription Initiation Site ; Virgibacillus ; Virgibacillus - genetics ; Virgibacillus - metabolism ; Virgibacillus - physiology ; Virgibacillus pantothenticus</subject><ispartof>Journal of Bacteriology, 2011-09, Vol.193 (18), p.4699-4708</ispartof><rights>2015 INIST-CNRS</rights><rights>Copyright © 2011, American Society for Microbiology. All Rights Reserved.</rights><rights>Copyright American Society for Microbiology Sep 2011</rights><rights>Copyright © 2011, American Society for Microbiology. All Rights Reserved. 2011 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c563t-20e54c39e875e9a03d0148d27979f4b4393f1a330397c2149ae0cb107c7a3ddd3</citedby><cites>FETCH-LOGICAL-c563t-20e54c39e875e9a03d0148d27979f4b4393f1a330397c2149ae0cb107c7a3ddd3</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/PMC3165649/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3165649/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24504694$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21764932$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuhlmann, Anne U</creatorcontrib><creatorcontrib>Hoffmann, Tamara</creatorcontrib><creatorcontrib>Bursy, Jan</creatorcontrib><creatorcontrib>Jebbar, Mohamed</creatorcontrib><creatorcontrib>Bremer, Erhard</creatorcontrib><title>Ectoine and Hydroxyectoine as Protectants against Osmotic and Cold Stress: Uptake through the SigB-Controlled Betaine-Choline- Carnitine Transporter-Type Carrier EctT from Virgibacillus pantothenticus</title><title>Journal of Bacteriology</title><addtitle>J Bacteriol</addtitle><description>Virgibacillus pantothenticus has been shown to synthesize the compatible solute ectoine in response to high salinity or low growth temperature. We found that exogenously provided ectoine and hydroxyectoine also serve as protectants against these challenges. Transport studies with [14C]ectoine revealed that both types of stress induced a high-affinity ectoine uptake activity in V. pantothenticus. By using an Escherichia coli mutant defective in osmoprotectant uptake systems, a functional complementation approach for osmostress resistance in the presence of ectoine was employed to retrieve a gene encoding an ectoine transporter from V. pantothenticus. The cloned gene (ectT) encodes a protein (EctT) that is a member of the BCCT (betaine-choline-carnitine-transporter) family of carriers. Osmoprotection assays demonstrated that the EctT carrier mediates the preferential import of ectoine and hydroxyectoine but also possesses minor uptake activities for the compatible solutes proline and glycine betaine. Northern blot analysis with RNA isolated from V. pantothenticus revealed that a rise in the external osmolality or a reduction in growth temperature strongly increased the transcription of the ectT gene. Primer extension analysis demonstrated that ectT was transcribed under these conditions from a SigB-type promoter. SigB is the master regulator of the general stress regulon of bacilli and provides protection to cells against various challenges, including high salinity and low temperature. Both the synthesis of ectoine and the EctT-mediated uptake of ectoine and hydroxyectoine are triggered by the same environmental cues, high salinity and cold stress, and thereby provide, in a concerted fashion, the protection of V. pantothenticus against these challenges.</description><subject>Abiotic stress</subject><subject>Amino Acids, Diamino</subject><subject>Amino Acids, Diamino - metabolism</subject><subject>Bacterial Proteins</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>betaine</subject><subject>Biological and medical sciences</subject><subject>Blotting, Northern</subject><subject>Carbon Radioisotopes</subject><subject>Carbon Radioisotopes - metabolism</subject><subject>carnitine</subject><subject>Chemical compounds</subject><subject>chemistry</subject><subject>Cloning</subject><subject>cold stress</subject><subject>cold tolerance</subject><subject>Cold-Shock Response</subject><subject>DNA, Bacterial</subject><subject>DNA, Bacterial - chemistry</subject><subject>DNA, Bacterial - genetics</subject><subject>Drug resistance</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genetic Complementation Test</subject><subject>genetics</subject><subject>growth retardation</subject><subject>Membrane Transport Proteins</subject><subject>Membrane Transport Proteins - genetics</subject><subject>Membrane Transport Proteins - metabolism</subject><subject>metabolism</subject><subject>methods</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>Molecular Sequence Data</subject><subject>mutants</subject><subject>Mutation</subject><subject>Northern blotting</subject><subject>osmolality</subject><subject>Osmotic Pressure</subject><subject>osmotic stress</subject><subject>osmotolerance</subject><subject>physiology</subject><subject>Physiology and Metabolism</subject><subject>proline</subject><subject>regulon</subject><subject>RNA</subject><subject>salinity</subject><subject>Sequence Analysis, DNA</subject><subject>Sigma Factor</subject><subject>Sigma Factor - metabolism</subject><subject>solutes</subject><subject>Staining and Labeling</subject><subject>Staining and Labeling - methods</subject><subject>Stress, Physiological</subject><subject>Substrate Specificity</subject><subject>temperature</subject><subject>Transcription Initiation Site</subject><subject>Virgibacillus</subject><subject>Virgibacillus - genetics</subject><subject>Virgibacillus - metabolism</subject><subject>Virgibacillus - physiology</subject><subject>Virgibacillus pantothenticus</subject><issn>0021-9193</issn><issn>1098-5530</issn><issn>1067-8832</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kk1v1DAQhiMEomXhxB2sSggklOLPJOaAxEaFUlUq0u5ytbyOk3hJ4sV2gP2H_Cyc7rYFDsiHkT2P33k9niR5iuApQrh4czE_hQznMEXoXnKMIC9Sxgi8nxxDiFHKESdHySPvNxAiShl-mBxhlGeUE3yc_DpTwZpBAzlU4HxXOftzp2-OPPjsbIhbOQQPZCPN4AO48r0NRl3fKG1XgUVw2vu3YLUN8qsGoXV2bNoYNViYZp6WdgjOdp2uwFyHKKLTsrXdFEEp3WDCVG3p5OC31gXt0uVuq6eUM9qB6HAJamd78MW4xqylMl03erCNrmwsMkQzo3-cPKhl5_WTQ5wlqw9ny_I8vbz6-Kl8f5kqlpGQYqgZVYTrImeaS0iq2JSiwjnPeU3XlHBSI0kIJDxXGFEuNVRrBHOVS1JVFZkl7_a623Hd60rF8k52YutML91OWGnE35nBtKKx3wVBGZuaPkteHgSc_TZqH0RvvNJdJwdtRy-KgrEMZxmO5Kv_kijLSFwsRxE9-Qfd2NENsRFRL2eEwQJG6PUeUs5673R96xpBMY2SuJiL61GKu0g_-_Oht-zN7ETgxQGQXsmujv-njL_jKIM04_TOW2ua9odxWkjfi81axMEUqBARmrryfA_V0grZuCi0WmCIGISQI8oo-Q1yhOkE</recordid><startdate>20110901</startdate><enddate>20110901</enddate><creator>Kuhlmann, Anne U</creator><creator>Hoffmann, Tamara</creator><creator>Bursy, Jan</creator><creator>Jebbar, Mohamed</creator><creator>Bremer, Erhard</creator><general>American Society for Microbiology</general><scope>FBQ</scope><scope>IQODW</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>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7S9</scope><scope>L.6</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20110901</creationdate><title>Ectoine and Hydroxyectoine as Protectants against Osmotic and Cold Stress: Uptake through the SigB-Controlled Betaine-Choline- Carnitine Transporter-Type Carrier EctT from Virgibacillus pantothenticus</title><author>Kuhlmann, Anne U ; Hoffmann, Tamara ; Bursy, Jan ; Jebbar, Mohamed ; Bremer, Erhard</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c563t-20e54c39e875e9a03d0148d27979f4b4393f1a330397c2149ae0cb107c7a3ddd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Abiotic stress</topic><topic>Amino Acids, Diamino</topic><topic>Amino Acids, Diamino - metabolism</topic><topic>Bacterial Proteins</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>betaine</topic><topic>Biological and medical sciences</topic><topic>Blotting, Northern</topic><topic>Carbon Radioisotopes</topic><topic>Carbon Radioisotopes - metabolism</topic><topic>carnitine</topic><topic>Chemical compounds</topic><topic>chemistry</topic><topic>Cloning</topic><topic>cold stress</topic><topic>cold tolerance</topic><topic>Cold-Shock Response</topic><topic>DNA, Bacterial</topic><topic>DNA, Bacterial - chemistry</topic><topic>DNA, Bacterial - genetics</topic><topic>Drug resistance</topic><topic>E coli</topic><topic>Escherichia coli</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - metabolism</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genetic Complementation Test</topic><topic>genetics</topic><topic>growth retardation</topic><topic>Membrane Transport Proteins</topic><topic>Membrane Transport Proteins - genetics</topic><topic>Membrane Transport Proteins - metabolism</topic><topic>metabolism</topic><topic>methods</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>Molecular Sequence Data</topic><topic>mutants</topic><topic>Mutation</topic><topic>Northern blotting</topic><topic>osmolality</topic><topic>Osmotic Pressure</topic><topic>osmotic stress</topic><topic>osmotolerance</topic><topic>physiology</topic><topic>Physiology and Metabolism</topic><topic>proline</topic><topic>regulon</topic><topic>RNA</topic><topic>salinity</topic><topic>Sequence Analysis, DNA</topic><topic>Sigma Factor</topic><topic>Sigma Factor - metabolism</topic><topic>solutes</topic><topic>Staining and Labeling</topic><topic>Staining and Labeling - methods</topic><topic>Stress, Physiological</topic><topic>Substrate Specificity</topic><topic>temperature</topic><topic>Transcription Initiation Site</topic><topic>Virgibacillus</topic><topic>Virgibacillus - genetics</topic><topic>Virgibacillus - metabolism</topic><topic>Virgibacillus - physiology</topic><topic>Virgibacillus pantothenticus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuhlmann, Anne U</creatorcontrib><creatorcontrib>Hoffmann, Tamara</creatorcontrib><creatorcontrib>Bursy, Jan</creatorcontrib><creatorcontrib>Jebbar, Mohamed</creatorcontrib><creatorcontrib>Bremer, Erhard</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</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>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of Bacteriology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuhlmann, Anne U</au><au>Hoffmann, Tamara</au><au>Bursy, Jan</au><au>Jebbar, Mohamed</au><au>Bremer, Erhard</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ectoine and Hydroxyectoine as Protectants against Osmotic and Cold Stress: Uptake through the SigB-Controlled Betaine-Choline- Carnitine Transporter-Type Carrier EctT from Virgibacillus pantothenticus</atitle><jtitle>Journal of Bacteriology</jtitle><addtitle>J Bacteriol</addtitle><date>2011-09-01</date><risdate>2011</risdate><volume>193</volume><issue>18</issue><spage>4699</spage><epage>4708</epage><pages>4699-4708</pages><issn>0021-9193</issn><eissn>1098-5530</eissn><eissn>1067-8832</eissn><coden>JOBAAY</coden><abstract>Virgibacillus pantothenticus has been shown to synthesize the compatible solute ectoine in response to high salinity or low growth temperature. We found that exogenously provided ectoine and hydroxyectoine also serve as protectants against these challenges. Transport studies with [14C]ectoine revealed that both types of stress induced a high-affinity ectoine uptake activity in V. pantothenticus. By using an Escherichia coli mutant defective in osmoprotectant uptake systems, a functional complementation approach for osmostress resistance in the presence of ectoine was employed to retrieve a gene encoding an ectoine transporter from V. pantothenticus. The cloned gene (ectT) encodes a protein (EctT) that is a member of the BCCT (betaine-choline-carnitine-transporter) family of carriers. Osmoprotection assays demonstrated that the EctT carrier mediates the preferential import of ectoine and hydroxyectoine but also possesses minor uptake activities for the compatible solutes proline and glycine betaine. Northern blot analysis with RNA isolated from V. pantothenticus revealed that a rise in the external osmolality or a reduction in growth temperature strongly increased the transcription of the ectT gene. Primer extension analysis demonstrated that ectT was transcribed under these conditions from a SigB-type promoter. SigB is the master regulator of the general stress regulon of bacilli and provides protection to cells against various challenges, including high salinity and low temperature. Both the synthesis of ectoine and the EctT-mediated uptake of ectoine and hydroxyectoine are triggered by the same environmental cues, high salinity and cold stress, and thereby provide, in a concerted fashion, the protection of V. pantothenticus against these challenges.</abstract><cop>Washington, DC</cop><pub>American Society for Microbiology</pub><pmid>21764932</pmid><doi>10.1128/JB.05270-11</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
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| ispartof | Journal of Bacteriology, 2011-09, Vol.193 (18), p.4699-4708 |
| issn | 0021-9193 1098-5530 1067-8832 |
| language | eng |
| recordid | cdi_highwire_asm_jb_193_18_4699 |
| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Abiotic stress Amino Acids, Diamino Amino Acids, Diamino - metabolism Bacterial Proteins Bacterial Proteins - metabolism Bacteriology betaine Biological and medical sciences Blotting, Northern Carbon Radioisotopes Carbon Radioisotopes - metabolism carnitine Chemical compounds chemistry Cloning cold stress cold tolerance Cold-Shock Response DNA, Bacterial DNA, Bacterial - chemistry DNA, Bacterial - genetics Drug resistance E coli Escherichia coli Escherichia coli - genetics Escherichia coli - metabolism Fundamental and applied biological sciences. Psychology Gene Expression Profiling Gene Expression Regulation, Bacterial Genetic Complementation Test genetics growth retardation Membrane Transport Proteins Membrane Transport Proteins - genetics Membrane Transport Proteins - metabolism metabolism methods Microbiology Miscellaneous Molecular Sequence Data mutants Mutation Northern blotting osmolality Osmotic Pressure osmotic stress osmotolerance physiology Physiology and Metabolism proline regulon RNA salinity Sequence Analysis, DNA Sigma Factor Sigma Factor - metabolism solutes Staining and Labeling Staining and Labeling - methods Stress, Physiological Substrate Specificity temperature Transcription Initiation Site Virgibacillus Virgibacillus - genetics Virgibacillus - metabolism Virgibacillus - physiology Virgibacillus pantothenticus |
| title | Ectoine and Hydroxyectoine as Protectants against Osmotic and Cold Stress: Uptake through the SigB-Controlled Betaine-Choline- Carnitine Transporter-Type Carrier EctT from Virgibacillus pantothenticus |
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