Changes in translational efficiency is a dominant regulatory mechanism in the environmental response of bacteria
To understand how cell physiological state affects mRNA translation, we used Shewanella oneidensis MR-1 grown under steady state conditions at either 20% or 8.5% O2. Using a combination of quantitative proteomics and RNA-Seq, we generated high-confidence data on >1000 mRNA and protein pairs. By u...
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| Veröffentlicht in: | Integrative Biology, 5(11):1393-1406 5(11):1393-1406, 2013-01, Vol.5 (11), p.1393-1406 |
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| container_title | Integrative Biology, 5(11):1393-1406 |
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| creator | Taylor, Ronald C Webb Robertson, Bobbie-Jo M Markillie, Lye Meng Serres, Margrethe H Linggi, Bryan E Aldrich, Joshua T Hill, Eric A Romine, Margaret F Lipton, Mary S Wiley, H Steven |
| description | To understand how cell physiological state affects mRNA translation, we used Shewanella oneidensis MR-1 grown under steady state conditions at either 20% or 8.5% O2. Using a combination of quantitative proteomics and RNA-Seq, we generated high-confidence data on >1000 mRNA and protein pairs. By using a steady state model, we found that differences in protein-mRNA ratios were primarily due to differences in the translational efficiency of specific genes. When oxygen levels were lowered, 28% of the proteins showed at least a 2-fold change in expression. Transcription levels were sp. significantly altered for 26% of the protein changes; translational efficiency was significantly altered for 46% and a combination of both was responsible for the remaining 28%. Changes in translational efficiency were significantly correlated with the codon usage pattern of the genes and measurable tRNA pools changed in response to altered O2 levels. Our results suggest that changes in the translational efficiency of proteins, in part due to altered tRNA pools, is a major determinant of regulated alterations in protein expression levels in bacteria. |
| doi_str_mv | 10.1039/c3ib40120k |
| format | Article |
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Using a combination of quantitative proteomics and RNA-Seq, we generated high-confidence data on >1000 mRNA and protein pairs. By using a steady state model, we found that differences in protein-mRNA ratios were primarily due to differences in the translational efficiency of specific genes. When oxygen levels were lowered, 28% of the proteins showed at least a 2-fold change in expression. Transcription levels were sp. significantly altered for 26% of the protein changes; translational efficiency was significantly altered for 46% and a combination of both was responsible for the remaining 28%. Changes in translational efficiency were significantly correlated with the codon usage pattern of the genes and measurable tRNA pools changed in response to altered O2 levels. Our results suggest that changes in the translational efficiency of proteins, in part due to altered tRNA pools, is a major determinant of regulated alterations in protein expression levels in bacteria.</description><subject>Bacterial Physiological Phenomena</subject><subject>Bacterial Proteins - metabolism</subject><subject>Codon</subject><subject>Environment</subject><subject>Environmental Molecular Sciences Laboratory</subject><subject>Escherichia coli - metabolism</subject><subject>Mass Spectrometry</subject><subject>microbiology</subject><subject>Oxygen - metabolism</subject><subject>Protein Biosynthesis</subject><subject>Proteome</subject><subject>Proteomics</subject><subject>Regression Analysis</subject><subject>Reproducibility of Results</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA, Transfer - metabolism</subject><subject>Sequence Analysis, RNA</subject><subject>Shewanella - genetics</subject><subject>Shewanella - metabolism</subject><subject>Shewanella oneidensis</subject><subject>systems biology</subject><subject>Time Factors</subject><subject>Transcription, Genetic</subject><subject>Transcriptome</subject><subject>transcriptomics</subject><issn>1757-9694</issn><issn>1757-9708</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtrVDEUxy9isbW68QNIcCXC1LwfG6EMvqDQja5Dbu7JTPTeZEwyhfn2pk5bddXVOXB-538e_2F4RfAFwcy89yyOHBOKfz4ZzogSamUU1k_vc2n46fC81h8YS44xfzacUo414dScDbv11qUNVBQTasWlOrsWc3IzghCij5D8AcWKHJryEpNLDRXY7DuVywEt4Ht7rMuf9i0gSDex5LRAal2iQN3lVAHlgEbnG5ToXgwnwc0VXt7F8-H7p4_f1l9WV9efv64vr1aeM91WngqCw0jGEIRXShpmsDHEcErpaIhWMgQ-iSmoCSup5QjCASeeac1h5JSdDx-Ourv9uMDk-0bFzXZX4uLKwWYX7f-VFLd2k28sM1IbwbrAm6NAri3a6mPrx_qcEvhmCbl9IO7Q27spJf_aQ212idXDPLsEeV8tEVJqobQgj6Occ2YoN6aj746oL7nWAuFhbYLtreX2r-Udfv3voQ_ovcfsN6XOqRQ</recordid><startdate>20130101</startdate><enddate>20130101</enddate><creator>Taylor, Ronald C</creator><creator>Webb Robertson, Bobbie-Jo M</creator><creator>Markillie, Lye Meng</creator><creator>Serres, Margrethe H</creator><creator>Linggi, Bryan E</creator><creator>Aldrich, Joshua T</creator><creator>Hill, Eric A</creator><creator>Romine, Margaret F</creator><creator>Lipton, Mary S</creator><creator>Wiley, H Steven</creator><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>7X8</scope><scope>7QL</scope><scope>C1K</scope><scope>OTOTI</scope><scope>5PM</scope></search><sort><creationdate>20130101</creationdate><title>Changes in translational efficiency is a dominant regulatory mechanism in the environmental response of bacteria</title><author>Taylor, Ronald C ; Webb Robertson, Bobbie-Jo M ; Markillie, Lye Meng ; Serres, Margrethe H ; Linggi, Bryan E ; Aldrich, Joshua T ; Hill, Eric A ; Romine, Margaret F ; Lipton, Mary S ; Wiley, H Steven</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c438t-c2510fb1bff5c776939099194222b91876ff4d5df7d07686be5ae41c3884eb423</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Bacterial Physiological Phenomena</topic><topic>Bacterial Proteins - metabolism</topic><topic>Codon</topic><topic>Environment</topic><topic>Environmental Molecular Sciences Laboratory</topic><topic>Escherichia coli - metabolism</topic><topic>Mass Spectrometry</topic><topic>microbiology</topic><topic>Oxygen - metabolism</topic><topic>Protein Biosynthesis</topic><topic>Proteome</topic><topic>Proteomics</topic><topic>Regression Analysis</topic><topic>Reproducibility of Results</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA, Transfer - metabolism</topic><topic>Sequence Analysis, RNA</topic><topic>Shewanella - genetics</topic><topic>Shewanella - metabolism</topic><topic>Shewanella oneidensis</topic><topic>systems biology</topic><topic>Time Factors</topic><topic>Transcription, Genetic</topic><topic>Transcriptome</topic><topic>transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Taylor, Ronald C</creatorcontrib><creatorcontrib>Webb Robertson, Bobbie-Jo M</creatorcontrib><creatorcontrib>Markillie, Lye Meng</creatorcontrib><creatorcontrib>Serres, Margrethe H</creatorcontrib><creatorcontrib>Linggi, Bryan E</creatorcontrib><creatorcontrib>Aldrich, Joshua T</creatorcontrib><creatorcontrib>Hill, Eric A</creatorcontrib><creatorcontrib>Romine, Margaret F</creatorcontrib><creatorcontrib>Lipton, Mary S</creatorcontrib><creatorcontrib>Wiley, H Steven</creatorcontrib><creatorcontrib>Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environmental Sciences and Pollution Management</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Integrative Biology, 5(11):1393-1406</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Taylor, Ronald C</au><au>Webb Robertson, Bobbie-Jo M</au><au>Markillie, Lye Meng</au><au>Serres, Margrethe H</au><au>Linggi, Bryan E</au><au>Aldrich, Joshua T</au><au>Hill, Eric A</au><au>Romine, Margaret F</au><au>Lipton, Mary S</au><au>Wiley, H Steven</au><aucorp>Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Changes in translational efficiency is a dominant regulatory mechanism in the environmental response of bacteria</atitle><jtitle>Integrative Biology, 5(11):1393-1406</jtitle><addtitle>Integr Biol (Camb)</addtitle><date>2013-01-01</date><risdate>2013</risdate><volume>5</volume><issue>11</issue><spage>1393</spage><epage>1406</epage><pages>1393-1406</pages><issn>1757-9694</issn><eissn>1757-9708</eissn><abstract>To understand how cell physiological state affects mRNA translation, we used Shewanella oneidensis MR-1 grown under steady state conditions at either 20% or 8.5% O2. Using a combination of quantitative proteomics and RNA-Seq, we generated high-confidence data on >1000 mRNA and protein pairs. By using a steady state model, we found that differences in protein-mRNA ratios were primarily due to differences in the translational efficiency of specific genes. When oxygen levels were lowered, 28% of the proteins showed at least a 2-fold change in expression. Transcription levels were sp. significantly altered for 26% of the protein changes; translational efficiency was significantly altered for 46% and a combination of both was responsible for the remaining 28%. Changes in translational efficiency were significantly correlated with the codon usage pattern of the genes and measurable tRNA pools changed in response to altered O2 levels. 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| ispartof | Integrative Biology, 5(11):1393-1406, 2013-01, Vol.5 (11), p.1393-1406 |
| issn | 1757-9694 1757-9708 |
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| source | MEDLINE; Oxford University Press Journals All Titles (1996-Current); Royal Society Of Chemistry Journals 2008- |
| subjects | Bacterial Physiological Phenomena Bacterial Proteins - metabolism Codon Environment Environmental Molecular Sciences Laboratory Escherichia coli - metabolism Mass Spectrometry microbiology Oxygen - metabolism Protein Biosynthesis Proteome Proteomics Regression Analysis Reproducibility of Results RNA, Messenger - metabolism RNA, Transfer - metabolism Sequence Analysis, RNA Shewanella - genetics Shewanella - metabolism Shewanella oneidensis systems biology Time Factors Transcription, Genetic Transcriptome transcriptomics |
| title | Changes in translational efficiency is a dominant regulatory mechanism in the environmental response of bacteria |
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