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Autoregulation of the tufB operon in Salmonella
Summary In Salmonella enterica and related species, translation elongation factor EF‐Tu is encoded by two widely separated but near‐identical genes, tufA and tufB. Two thirds of EF‐Tu is expressed from tufA with the remaining one third coming from tufB. Inactivation of tufA is partly compensated by...
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Published in: | Molecular microbiology 2016-06, Vol.100 (6), p.1004-1016 |
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description | Summary
In Salmonella enterica and related species, translation elongation factor EF‐Tu is encoded by two widely separated but near‐identical genes, tufA and tufB. Two thirds of EF‐Tu is expressed from tufA with the remaining one third coming from tufB. Inactivation of tufA is partly compensated by a doubling in the amount of EF‐TuB but the mechanism of this up‐regulation is unknown. By experimental evolution selecting for improved growth rate in a strain with an inactive tufA we selected six different noncoding or synonymous point mutations close to the tufB start codon. Based on these results we constructed a total of 161 different point mutations around the tufB start codon, as well as tufB 3′‐truncations, and measured tufB expression using tufB‐yfp transcriptional and translational fusions. The expression data support the presence of two competing stem‐loop structures that can form in the 5′‐end of the tufB mRNA. Formation of the ‘closed’ structure leads to Rho‐dependent transcriptional termination of the tufB mRNA. We propose a model in which translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated.
The amount of EF‐Tu expressed from tufB can vary two‐fold but the mechanism of this regulation is unknown. Based on analysis of selected and constructed mutations, and using transcriptional and translational fusions, we propose a model where translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated. |
doi_str_mv | 10.1111/mmi.13364 |
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In Salmonella enterica and related species, translation elongation factor EF‐Tu is encoded by two widely separated but near‐identical genes, tufA and tufB. Two thirds of EF‐Tu is expressed from tufA with the remaining one third coming from tufB. Inactivation of tufA is partly compensated by a doubling in the amount of EF‐TuB but the mechanism of this up‐regulation is unknown. By experimental evolution selecting for improved growth rate in a strain with an inactive tufA we selected six different noncoding or synonymous point mutations close to the tufB start codon. Based on these results we constructed a total of 161 different point mutations around the tufB start codon, as well as tufB 3′‐truncations, and measured tufB expression using tufB‐yfp transcriptional and translational fusions. The expression data support the presence of two competing stem‐loop structures that can form in the 5′‐end of the tufB mRNA. Formation of the ‘closed’ structure leads to Rho‐dependent transcriptional termination of the tufB mRNA. We propose a model in which translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated.
The amount of EF‐Tu expressed from tufB can vary two‐fold but the mechanism of this regulation is unknown. Based on analysis of selected and constructed mutations, and using transcriptional and translational fusions, we propose a model where translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated.</description><identifier>ISSN: 0950-382X</identifier><identifier>ISSN: 1365-2958</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.13364</identifier><identifier>PMID: 26934594</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Bacterial Proteins ; Biologi med inriktning mot mikrobiologi ; Biology with specialization in Microbiology ; EF-Tu ; Escherichia coli - genetics ; Escherichia coli - metabolism ; Genes ; Genes, Bacterial ; Homeostasis ; Microbiology ; Mikrobiologi ; Molecular Genetics ; Molekylär genetik ; Mutation ; Operon ; Peptide Elongation Factor Tu - genetics ; Peptide Elongation Factor Tu - metabolism ; Point Mutation ; post-transcriptional regulation ; Protein Biosynthesis ; Rho ; RNA, Bacterial - genetics ; RNA, Bacterial - metabolism ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Salmonella ; Salmonella - genetics ; Salmonella - metabolism ; Salmonella enterica ; Transcription, Genetic ; tufA ; tufB</subject><ispartof>Molecular microbiology, 2016-06, Vol.100 (6), p.1004-1016</ispartof><rights>2016 John Wiley & Sons Ltd</rights><rights>2016 John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4234-30671d517892281b8ed2dc3c5d63582c006ddc4315aaeeb471bd6d14939862b93</citedby><cites>FETCH-LOGICAL-c4234-30671d517892281b8ed2dc3c5d63582c006ddc4315aaeeb471bd6d14939862b93</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/26934594$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-235218$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Brandis, Gerrit</creatorcontrib><creatorcontrib>Bergman, Jessica M.</creatorcontrib><creatorcontrib>Hughes, Diarmaid</creatorcontrib><title>Autoregulation of the tufB operon in Salmonella</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
In Salmonella enterica and related species, translation elongation factor EF‐Tu is encoded by two widely separated but near‐identical genes, tufA and tufB. Two thirds of EF‐Tu is expressed from tufA with the remaining one third coming from tufB. Inactivation of tufA is partly compensated by a doubling in the amount of EF‐TuB but the mechanism of this up‐regulation is unknown. By experimental evolution selecting for improved growth rate in a strain with an inactive tufA we selected six different noncoding or synonymous point mutations close to the tufB start codon. Based on these results we constructed a total of 161 different point mutations around the tufB start codon, as well as tufB 3′‐truncations, and measured tufB expression using tufB‐yfp transcriptional and translational fusions. The expression data support the presence of two competing stem‐loop structures that can form in the 5′‐end of the tufB mRNA. Formation of the ‘closed’ structure leads to Rho‐dependent transcriptional termination of the tufB mRNA. We propose a model in which translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated.
The amount of EF‐Tu expressed from tufB can vary two‐fold but the mechanism of this regulation is unknown. Based on analysis of selected and constructed mutations, and using transcriptional and translational fusions, we propose a model where translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated.</description><subject>Bacterial Proteins</subject><subject>Biologi med inriktning mot mikrobiologi</subject><subject>Biology with specialization in Microbiology</subject><subject>EF-Tu</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - metabolism</subject><subject>Genes</subject><subject>Genes, Bacterial</subject><subject>Homeostasis</subject><subject>Microbiology</subject><subject>Mikrobiologi</subject><subject>Molecular Genetics</subject><subject>Molekylär genetik</subject><subject>Mutation</subject><subject>Operon</subject><subject>Peptide Elongation Factor Tu - genetics</subject><subject>Peptide Elongation Factor Tu - metabolism</subject><subject>Point Mutation</subject><subject>post-transcriptional regulation</subject><subject>Protein Biosynthesis</subject><subject>Rho</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA, Bacterial - metabolism</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Salmonella</subject><subject>Salmonella - genetics</subject><subject>Salmonella - metabolism</subject><subject>Salmonella enterica</subject><subject>Transcription, Genetic</subject><subject>tufA</subject><subject>tufB</subject><issn>0950-382X</issn><issn>1365-2958</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNqF0U1LwzAcBvAgis6Xg19ACl4U7Jb3Jsc5X8HhwRe8hbbJtNI2M2kYfnszO3cQxFwC4ceT5P8AcIjgEMU1appqiAjhdAMMEOEsxZKJTTCAksGUCPyyA3a9f4cQEcjJNtjBXBLKJB2A0Th01pnXUOddZdvEzpLuzSRdmJ0ndm5cPKra5CGvG9uaus73wdYsr705WO174Onq8nFyk97dX99OxndpSTGhabwnQ5qhTEiMBSqE0ViXpGSaEyZwCSHXuqQEsTw3pqAZKjTXiEoiBceFJHvgrM_1CzMPhZq7qsndp7J5pS6q57Gy7lWFoDBhGInIT3o-d_YjGN-ppvLl8sGtscErJHAmRJxN9j_N4vAyRiSP9PgXfbfBtfHfS0URwhLiqE57VTrrvTOz9WMRVMt-VOxHffcT7dEqMRSN0Wv5U0gEox4sqtp8_p2kptPbPvILshOWUg</recordid><startdate>201606</startdate><enddate>201606</enddate><creator>Brandis, Gerrit</creator><creator>Bergman, Jessica M.</creator><creator>Hughes, Diarmaid</creator><general>Blackwell Publishing Ltd</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</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>7X8</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>DF2</scope></search><sort><creationdate>201606</creationdate><title>Autoregulation of the tufB operon in Salmonella</title><author>Brandis, Gerrit ; Bergman, Jessica M. ; Hughes, Diarmaid</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4234-30671d517892281b8ed2dc3c5d63582c006ddc4315aaeeb471bd6d14939862b93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Bacterial Proteins</topic><topic>Biologi med inriktning mot mikrobiologi</topic><topic>Biology with specialization in Microbiology</topic><topic>EF-Tu</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - metabolism</topic><topic>Genes</topic><topic>Genes, Bacterial</topic><topic>Homeostasis</topic><topic>Microbiology</topic><topic>Mikrobiologi</topic><topic>Molecular Genetics</topic><topic>Molekylär genetik</topic><topic>Mutation</topic><topic>Operon</topic><topic>Peptide Elongation Factor Tu - genetics</topic><topic>Peptide Elongation Factor Tu - metabolism</topic><topic>Point Mutation</topic><topic>post-transcriptional regulation</topic><topic>Protein Biosynthesis</topic><topic>Rho</topic><topic>RNA, Bacterial - genetics</topic><topic>RNA, Bacterial - metabolism</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Salmonella</topic><topic>Salmonella - genetics</topic><topic>Salmonella - metabolism</topic><topic>Salmonella enterica</topic><topic>Transcription, Genetic</topic><topic>tufA</topic><topic>tufB</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brandis, Gerrit</creatorcontrib><creatorcontrib>Bergman, Jessica M.</creatorcontrib><creatorcontrib>Hughes, Diarmaid</creatorcontrib><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>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</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>MEDLINE - Academic</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Uppsala universitet</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brandis, Gerrit</au><au>Bergman, Jessica M.</au><au>Hughes, Diarmaid</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Autoregulation of the tufB operon in Salmonella</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2016-06</date><risdate>2016</risdate><volume>100</volume><issue>6</issue><spage>1004</spage><epage>1016</epage><pages>1004-1016</pages><issn>0950-382X</issn><issn>1365-2958</issn><eissn>1365-2958</eissn><abstract>Summary
In Salmonella enterica and related species, translation elongation factor EF‐Tu is encoded by two widely separated but near‐identical genes, tufA and tufB. Two thirds of EF‐Tu is expressed from tufA with the remaining one third coming from tufB. Inactivation of tufA is partly compensated by a doubling in the amount of EF‐TuB but the mechanism of this up‐regulation is unknown. By experimental evolution selecting for improved growth rate in a strain with an inactive tufA we selected six different noncoding or synonymous point mutations close to the tufB start codon. Based on these results we constructed a total of 161 different point mutations around the tufB start codon, as well as tufB 3′‐truncations, and measured tufB expression using tufB‐yfp transcriptional and translational fusions. The expression data support the presence of two competing stem‐loop structures that can form in the 5′‐end of the tufB mRNA. Formation of the ‘closed’ structure leads to Rho‐dependent transcriptional termination of the tufB mRNA. We propose a model in which translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated.
The amount of EF‐Tu expressed from tufB can vary two‐fold but the mechanism of this regulation is unknown. Based on analysis of selected and constructed mutations, and using transcriptional and translational fusions, we propose a model where translational speed is used as a sensor for EF‐Tu concentration and where the expression of tufB is post‐transcriptionally regulated. This model describes for the first time how expression of the most abundant Salmonella protein is autoregulated.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>26934594</pmid><doi>10.1111/mmi.13364</doi><tpages>13</tpages></addata></record> |
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subjects | Bacterial Proteins Biologi med inriktning mot mikrobiologi Biology with specialization in Microbiology EF-Tu Escherichia coli - genetics Escherichia coli - metabolism Genes Genes, Bacterial Homeostasis Microbiology Mikrobiologi Molecular Genetics Molekylär genetik Mutation Operon Peptide Elongation Factor Tu - genetics Peptide Elongation Factor Tu - metabolism Point Mutation post-transcriptional regulation Protein Biosynthesis Rho RNA, Bacterial - genetics RNA, Bacterial - metabolism RNA, Messenger - genetics RNA, Messenger - metabolism Salmonella Salmonella - genetics Salmonella - metabolism Salmonella enterica Transcription, Genetic tufA tufB |
title | Autoregulation of the tufB operon in Salmonella |
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