Transcript level and sequence determinants of protein abundance and noise in Escherichia coli

Guimaraes, Joao C.; Rocha, Miguel; Arkin, Adam P.

doi:10.1093/nar/gku126

Title: Transcript level and sequence determinants of protein abundance and noise in Escherichia coli

Journal Article · Thu Feb 06 00:00:00 EST 2014 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gku126· OSTI ID:1625533

Guimaraes, Joao C. ^[1]; Rocha, Miguel ^[2]; Arkin, Adam P. ^[3]

Univ. of California, Berkeley, CA (United States); Univ. of Minho, Braga (Portugal)
Univ. of Minho, Braga (Portugal)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

The range over which a protein is expressed, and its cell-to-cell variability, is often thought to be linked to the demand for its activity. Steady-state protein level is determined by multiple mechanisms controlling transcription and translation, many of which are limited by DNA- and RNA-encoded signals that affect initiation, elongation and termination of polymerases and ribosomes. We performed a comprehensive analysis of >100 sequence features to derive a predictive model composed of a minimal non-redundant set of factors explaining 66% of the total variation of protein abundance observed in >800 genes in Escherichia coli. The model suggests that protein abundance is primarily determined by the transcript level (53%) and by effectors of translation elongation (12%), whereas only a small fraction of the variation is explained by translational initiation (1%). Our analyses uncover a new sequence determinant, not previously described, affecting translation initiation and suggest that elongation rate is affected by both codon biases and specific amino acid composition. We also show that transcription and translation efficiency may have an effect on expression noise, which is more similar than previously assumed.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625533

Journal Information:: Nucleic Acids Research, Vol. 42, Issue 8; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation Lu, Peng; Vogel, Christine; Wang, Rong Nature Biotechnology, Vol. 25, Issue 1 https://doi.org/10.1038/nbt1270	journal	December 2006
Synonymous codon bias is related to gene length in Escherichia coli: selection for translational accuracy? Eyre-Walker, A. Molecular Biology and Evolution, Vol. 13, Issue 6 https://doi.org/10.1093/oxfordjournals.molbev.a025646	journal	July 1996
Mechanisms of Attenuation by Genetic Recoding of Viruses Gonçalves-Carneiro, Daniel; Bieniasz, Paul D. mBio, Vol. 12, Issue 1 https://doi.org/10.1128/mbio.02238-20	journal	February 2021
Synonymous but not the same: the causes and consequences of codon bias Plotkin, Joshua B.; Kudla, Grzegorz Nature Reviews Genetics, Vol. 12, Issue 1 https://doi.org/10.1038/nrg2899	journal	November 2010
Data Mining with Neural Networks and Support Vector Machines Using the R/rminer Tool Cortez, Paulo Advances in Data Mining. Applications and Theoretical Aspects https://doi.org/10.1007/978-3-642-14400-4_44	book	January 2010
An Evolutionarily Conserved Mechanism for Controlling the Efficiency of Protein Translation Tuller, Tamir; Carmi, Asaf; Vestsigian, Kalin Cell, Vol. 141, Issue 2 https://doi.org/10.1016/j.cell.2010.03.031	journal	April 2010
Unfolding of mRNA Secondary Structure by the Bacterial Translation Initiation Complex Studer, Sean M.; Joseph, Simpson Molecular Cell, Vol. 22, Issue 1 https://doi.org/10.1016/j.molcel.2006.02.014	journal	April 2006
Translation initiation in Escherichia coli: sequences within the ribosome-binding site Ringquist, Steven; Shinedling, Sidney; Barrick, Doug Molecular Microbiology, Vol. 6, Issue 9 https://doi.org/10.1111/j.1365-2958.1992.tb01561.x	journal	May 1992
Lost in translation: the influence of ribosomes on bacterial mRNA decay Deana, A. Genes & Development, Vol. 19, Issue 21 https://doi.org/10.1101/gad.1348805	journal	November 2005
Stochasticity in gene expression: from theories to phenotypes Kærn, Mads; Elston, Timothy C.; Blake, William J. Nature Reviews Genetics, Vol. 6, Issue 6 https://doi.org/10.1038/nrg1615	journal	May 2005
Coding-Sequence Determinants of Gene Expression in Escherichia coli Kudla, G.; Murray, A. W.; Tollervey, D. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1170160	journal	April 2009
Quantifying E. coli Proteome and Transcriptome with Single-Molecule Sensitivity in Single Cells Taniguchi, Y.; Choi, P. J.; Li, G. -W. Science, Vol. 329, Issue 5991 https://doi.org/10.1126/science.1188308	journal	July 2010
Translation efficiency is determined by both codon bias and folding energy Tuller, Tamir; Waldman, Yedael Y.; Kupiec, Martin Proceedings of the National Academy of Sciences, Vol. 107, Issue 8 https://doi.org/10.1073/pnas.0909910107	journal	February 2010
The pls Package: Principal Component and Partial Least Squares Regression in R Mevik, Bjørn-Helge; Wehrens, Ron Journal of Statistical Software, Vol. 18, Issue 2 https://doi.org/10.18637/jss.v018.i02	journal	January 2007
Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. de Smit, M. H.; van Duin, J. Proceedings of the National Academy of Sciences, Vol. 87, Issue 19 https://doi.org/10.1073/pnas.87.19.7668	journal	October 1990
Translation is a non-uniform process Varenne, Stanislas; Buc, Jean; Lloubes, Roland Journal of Molecular Biology, Vol. 180, Issue 3 https://doi.org/10.1016/0022-2836(84)90027-5	journal	December 1984
Diverse molecular mechanisms of translation initiation in prokaryotes Boni, I. V. Molecular Biology, Vol. 40, Issue 4 https://doi.org/10.1134/S002689330604011X	journal	July 2006
Quantification of protein half-lives in the budding yeast proteome Belle, A.; Tanay, A.; Bitincka, L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 35 https://doi.org/10.1073/pnas.0605420103	journal	August 2006
Multifactorial Determinants of Protein Expression in Prokaryotic Open Reading Frames Allert, Malin; Cox, J. Colin; Hellinga, Homme W. Journal of Molecular Biology, Vol. 402, Issue 5 https://doi.org/10.1016/j.jmb.2010.08.010	journal	October 2010
Determination of the optimal aligned spacing between the Shine – Dalgarno sequence and the translation initiation codon of Escherichia coli m RNAs Chen, Hongyun; Bjerknes, Matthew; Kumar, Ravindra Nucleic Acids Research, Vol. 22, Issue 23 https://doi.org/10.1093/nar/22.23.4953	journal	January 1994
Posttranscriptional Expression Regulation: What Determines Translation Rates? Brockmann, Regina; Beyer, Andreas; Heinisch, Jürgen J. PLoS Computational Biology, Vol. 3, Issue 3 https://doi.org/10.1371/journal.pcbi.0030057	journal	January 2007
Proteomic and Transcriptomic Analyses Reveal Pathological Changes in the Entorhinal Cortex Region that Correlate Well with Dysregulation of Ion Transport in Patients with Alzheimer’s Disease Jia, Yangjie; Wang, Xia; Chen, Yanyu Molecular Neurobiology, Vol. 58, Issue 8 https://doi.org/10.1007/s12035-021-02356-3	journal	April 2021
Quantitative analysis of ribosome binding sites in E.coli Barrick, Doug; Villanueba, Keith; Childs, John Nucleic Acids Research, Vol. 22, Issue 7 https://doi.org/10.1093/nar/22.7.1287	journal	January 1994
Codon preferences in free-living microorganisms. Andersson, S. G.; Kurland, C. G. Microbiological Reviews, Vol. 54, Issue 2 https://doi.org/10.1128/MMBR.54.2.198-210.1990	journal	January 1990
Codon bias and heterologous protein expression Gustafsson, Claes; Govindarajan, Sridhar; Minshull, Jeremy Trends in Biotechnology, Vol. 22, Issue 7 https://doi.org/10.1016/j.tibtech.2004.04.006	journal	July 2004
Control of Translation by mRNA Secondary Structure in Escherichia coli de Smit, Maarten H.; van Duin, Jan Journal of Molecular Biology, Vol. 244, Issue 2 https://doi.org/10.1006/jmbi.1994.1714	journal	November 1994
Quantification of mRNA and protein and integration with protein turnover in a bacterium Maier, Tobias; Schmidt, Alexander; Güell, Marc ETH Zurich https://doi.org/10.3929/ethz-b-000038553	text	January 2011
Sequence signatures and mRNA concentration can explain two‐thirds of protein abundance variation in a human cell line Vogel, Christine; de Sousa Abreu, Raquel; Ko, Daijin Molecular Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1038/msb.2010.59	journal	January 2010
Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Akashi, H. Genetics, Vol. 136, Issue 3 https://doi.org/10.1093/genetics/136.3.927	journal	March 1994
Translational Selection and Yeast Proteome Evolution Akashi, Hiroshi Genetics, Vol. 164, Issue 4 https://doi.org/10.1093/genetics/164.4.1291	journal	August 2003
The selection-mutation-drift theory of synonymous codon usage. Bulmer, M. Genetics, Vol. 129, Issue 3 https://doi.org/10.1093/genetics/129.3.897	journal	November 1991
A Handbook of Statistical Analyses using Stata Berry, Diane Journal of the Royal Statistical Society: Series A (Statistics in Society), Vol. 171, Issue 3 https://doi.org/10.1111/j.1467-985X.2008.00538_8.x	journal	June 2008
Co-variation of tRNA Abundance and Codon Usage inEscherichia coliat Different Growth Rates Dong, Hengjiang; Nilsson, Lars; Kurland, Charles G. Journal of Molecular Biology, Vol. 260, Issue 5 https://doi.org/10.1006/jmbi.1996.0428	journal	August 1996
Rate-Limiting Steps in Yeast Protein Translation Shah, Premal; Ding, Yang; Niemczyk, Malwina Cell, Vol. 153, Issue 7 https://doi.org/10.1016/j.cell.2013.05.049	journal	June 2013
Quantification of mRNA and protein and integration with protein turnover in a bacterium Maier, Tobias; Schmidt, Alexander; Güell, Marc Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.38	journal	January 2011
Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling Ingolia, N. T.; Ghaemmaghami, S.; Newman, J. R. S. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1168978	journal	April 2009
Post-transcriptional Expression Regulation in the Yeast Saccharomyces cerevisiae on a Genomic Scale Beyer, Andreas; Hollunder, Jens; Nasheuer, Heinz-Peter Molecular & Cellular Proteomics, Vol. 3, Issue 11 https://doi.org/10.1074/mcp.M400099-MCP200	journal	November 2004
A Handbook of Statistical Analyses Using Stata Wells, Martin T. Journal of the American Statistical Association, Vol. 96, Issue 453 https://doi.org/10.1198/jasa.2001.s390	journal	March 2001
Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis Akashi, Hiroshi; Gojobori, Takashi Proceedings of the National Academy of Sciences, Vol. 99, Issue 6 https://doi.org/10.1073/pnas.062526999	journal	March 2002
Natural selection on gene expression Gilad, Yoav; Oshlack, Alicia; Rifkin, Scott A. Trends in Genetics, Vol. 22, Issue 8 https://doi.org/10.1016/j.tig.2006.06.002	journal	August 2006
Design Parameters to Control Synthetic Gene Expression in Escherichia coli Welch, Mark; Govindarajan, Sridhar; Ness, Jon E. PLoS ONE, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pone.0007002	journal	September 2009
Coevolution of Codon Usage and tRNA Genes Leads to Alternative Stable States of Biased Codon Usage Higgs, P. G.; Ran, W. Molecular Biology and Evolution, Vol. 25, Issue 11 https://doi.org/10.1093/molbev/msn173	journal	August 2008
Insights into the regulation of protein abundance from proteomic and transcriptomic analyses Vogel, Christine; Marcotte, Edward M. Nature Reviews Genetics, Vol. 13, Issue 4 https://doi.org/10.1038/nrg3185	journal	March 2012
Regulation of noise in the expression of a single gene Ozbudak, Ertugrul M.; Thattai, Mukund; Kurtser, Iren Nature Genetics, Vol. 31, Issue 1 https://doi.org/10.1038/ng869	journal	April 2002
The influence of ribosome-binding-site elements on translational efficiency in Bacillus subtilis and Escherichia coli in vivo Vellanoweth, Robert Luis; Rabinowitz, Jesse C. Molecular Microbiology, Vol. 6, Issue 9 https://doi.org/10.1111/j.1365-2958.1992.tb01548.x	journal	May 1992
Levels of tRNAs in bacterial cells as affected by amino acid usage in proteins Yamao, Fumiaki; Andachi, Yoshiki; Muto, Akira Nucleic Acids Research, Vol. 19, Issue 22 https://doi.org/10.1093/nar/19.22.6119	journal	January 1991
Global quantification of mammalian gene expression control Schwanhäusser, Björn; Busse, Dorothea; Li, Na Nature, Vol. 473, Issue 7347 https://doi.org/10.1038/nature10098	journal	May 2011
A Role for Codon Order in Translation Dynamics Cannarozzi, Gina; Schraudolph, Nicol N.; Faty, Mahamadou Cell, Vol. 141, Issue 4 https://doi.org/10.1016/j.cell.2010.04.027	journal	May 2010
Control, exploitation and tolerance of intracellular noise Rao, Christopher V.; Wolf, Denise M.; Arkin, Adam P. Nature, Vol. 420, Issue 6912 https://doi.org/10.1038/nature01258	journal	November 2002
A Genome-Wide Analysis of Promoter-Mediated Phenotypic Noise in Escherichia coli Silander, Olin K.; Nikolic, Nela; Zaslaver, Alon PLoS Genetics, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pgen.1002443	journal	January 2012
Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise Newman, John R. S.; Ghaemmaghami, Sina; Ihmels, Jan Nature, Vol. 441, Issue 7095 https://doi.org/10.1038/nature04785	journal	May 2006
A Role for Codon Order in Translation Dynamics Cannarozzi, Gina; Schraudolph, Nicol N.; Faty, Mahamadou Cell, Vol. 141, Issue 2 https://doi.org/10.1016/j.cell.2010.02.036	journal	April 2010
Teasing Apart Translational and Transcriptional Components of Stochastic Variations in Eukaryotic Gene Expression Salari, Raheleh; Wojtowicz, Damian; Zheng, Jie PLoS Computational Biology, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pcbi.1002644	journal	August 2012
Determinants of translation efficiency and accuracy Gingold, Hila; Pilpel, Yitzhak Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.14	journal	January 2011
Noise in protein expression scales with natural protein abundance Bar-Even, Arren; Paulsson, Johan; Maheshri, Narendra Nature Genetics, Vol. 38, Issue 6 https://doi.org/10.1038/ng1807	journal	May 2006
A role for mRNA secondary structure in the control of translation initiation Hall, Michael N.; Gabay, Joëlle; Débarbouillé, Michel Nature, Vol. 295, Issue 5850 https://doi.org/10.1038/295616a0	journal	February 1982
Translation initiation region sequence preferences in Escherichia coli Vimberg, Vladimir; Tats, Age; Remm, Maido BMC Molecular Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2199-8-100	journal	January 2007
A Genome-Wide Analysis of Promoter-Mediated Phenotypic Noise in Escherichia coli K., Silander, Olin; Nela, Nikolic,; Alon, Zaslaver, ETH Zurich https://doi.org/10.3929/ethz-b-000047104	text	January 2012
Stochastic protein expression in individual cells at the single molecule level Cai, Long; Friedman, Nir; Xie, X. Sunney Nature, Vol. 440, Issue 7082 https://doi.org/10.1038/nature04599	journal	March 2006
Periconceptional nutrition with spineless cactus (Opuntia ficus-indica) improves metabolomic profiles and pregnancy outcomes in sheep Rosales-Nieto, César A.; Rodríguez-Aguilar, Maribel; Santiago-Hernandez, Francisco Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-86653-w	journal	March 2021
Identifying DNA and protein patterns with statistically significant alignments of multiple sequences Hertz, G. Z.; Stormo, G. D. Bioinformatics, Vol. 15, Issue 7 https://doi.org/10.1093/bioinformatics/15.7.563	journal	July 1999
Determinant of cistron specificity in bacterial ribosomes Shine, J.; Dalgarno, L. Nature, Vol. 254, Issue 5495 https://doi.org/10.1038/254034a0	journal	March 1975
Anatomy of Escherichia coli ribosome binding sites Shultzaberger, Ryan K.; Bucheimer, R. Elaine; Rudd, Kenneth E. Journal of Molecular Biology, Vol. 313, Issue 1, p. 215-228 https://doi.org/10.1006/jmbi.2001.5040	journal	October 2001
Analysis of mRNA expression and protein abundance data: an approach for the comparison of the enrichment of features in the cellular population of proteins and transcripts Greenbaum, D.; Jansen, R.; Gerstein, M. Bioinformatics, Vol. 18, Issue 4 https://doi.org/10.1093/bioinformatics/18.4.585	journal	April 2002
Correlation of mRNA Expression and Protein Abundance Affected by Multiple Sequence Features Related to Translational Efficiency in Desulfovibrio vulgaris : A Quantitative Analysis Nie, Lei; Wu, Gang; Zhang, Weiwen Genetics, Vol. 174, Issue 4 https://doi.org/10.1534/genetics.106.065862	journal	October 2006
The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications Sharp, Paul M.; Li, Wen-Hsiung Nucleic Acids Research, Vol. 15, Issue 3, p. 1281-1295 https://doi.org/10.1093/nar/15.3.1281	journal	January 1987
Automated design of synthetic ribosome binding sites to control protein expression Salis, Howard M.; Mirsky, Ethan A.; Voigt, Christopher A. Nature Biotechnology, Vol. 27, Issue 10, p. 946-950 https://doi.org/10.1038/nbt.1568	journal	October 2009
Intrinsic noise in gene regulatory networks Thattai, M.; van Oudenaarden, A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 15 https://doi.org/10.1073/pnas.151588598	journal	July 2001
Indirect and suboptimal control of gene expression is widespread in bacteria Price, Morgan N.; Deutschbauer, Adam M.; Skerker, Jeffrey M. Molecular Systems Biology, Vol. 9, Issue 1 https://doi.org/10.1038/msb.2013.16	journal	January 2013
Noise in eukaryotic gene expression Blake, William J.; KÆrn, Mads; Cantor, Charles R. Nature, Vol. 422, Issue 6932 https://doi.org/10.1038/nature01546	journal	April 2003
Determinants of Protein Abundance and Translation Efficiency in S. cerevisiae Tuller, Tamir; Kupiec, Martin; Ruppin, Eytan PLoS Computational Biology, Vol. 3, Issue 12 https://doi.org/10.1371/journal.pcbi.0030248	journal	December 2007
How the Sequence of a Gene Can Tune Its Translation Fredrick, Kurt; Ibba, Michael Cell, Vol. 141, Issue 2 https://doi.org/10.1016/j.cell.2010.03.033	journal	April 2010
Two-Step Selection of mRNAs in Initiation of Protein Synthesis Hauryliuk, Vasili; Ehrenberg, Mans Molecular Cell, Vol. 22, Issue 2 https://doi.org/10.1016/j.molcel.2006.04.004	journal	April 2006
Translation rate modification by preferential codon usage: Intragenic position effects Liljenström, Hans; von Heijne, Gunnar Journal of Theoretical Biology, Vol. 124, Issue 1 https://doi.org/10.1016/s0022-5193(87)80251-5	journal	January 1987
Codon usage and intragenic position Bulmer, Michael Journal of Theoretical Biology, Vol. 133, Issue 1 https://doi.org/10.1016/s0022-5193(88)80024-9	journal	July 1988
The dynamic RNA world de Souza, Natalie Nature Methods, Vol. 8, Issue 7 https://doi.org/10.1038/nmeth0711-536	journal	June 2011
Unbiased Quantitation of Escherichia coli Membrane Proteome Using Phase Transfer Surfactants Masuda, Takeshi; Saito, Natsumi; Tomita, Masaru Molecular & Cellular Proteomics, Vol. 8, Issue 12 https://doi.org/10.1074/mcp.m900240-mcp200	journal	December 2009
Codon usage and tRNA content in unicellular and multicellular organisms. Ikemura, T. Molecular Biology and Evolution, 13–34 https://doi.org/10.1093/oxfordjournals.molbev.a040335	journal	January 1985
Codon preferences in free-living microorganisms Andersson, S. G.; Kurland, C. G. Microbiological Reviews, Vol. 54, Issue 2 https://doi.org/10.1128/mr.54.2.198-210.1990	journal	June 1990

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