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Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent

Efficient and accurate protein synthesis is crucial for organismal survival in competitive environments. Translation efficiency (the number of proteins translated from a single mRNA in a given time period) is the combined result of differential translation initiation, elongation, and termination rat...

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Autores principales: Yang, Chuyue, Hockenberry, Adam J., Jewett, Michael C., Amaral, Luís A. N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100845/
https://www.ncbi.nlm.nih.gov/pubmed/27605518
http://dx.doi.org/10.1534/g3.116.032227
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author Yang, Chuyue
Hockenberry, Adam J.
Jewett, Michael C.
Amaral, Luís A. N.
author_facet Yang, Chuyue
Hockenberry, Adam J.
Jewett, Michael C.
Amaral, Luís A. N.
author_sort Yang, Chuyue
collection PubMed
description Efficient and accurate protein synthesis is crucial for organismal survival in competitive environments. Translation efficiency (the number of proteins translated from a single mRNA in a given time period) is the combined result of differential translation initiation, elongation, and termination rates. Previous research identified the Shine-Dalgarno (SD) sequence as a modulator of translation initiation in bacterial genes, while codon usage biases are frequently implicated as a primary determinant of elongation rate variation. Recent studies have suggested that SD sequences within coding sequences may negatively affect translation elongation speed, but this claim remains controversial. Here, we present a metric to quantify the prevalence of SD sequences in coding regions. We analyze hundreds of bacterial genomes and find that the coding sequences of highly expressed genes systematically contain fewer SD sequences than expected, yielding a robust correlation between the normalized occurrence of SD sites and protein abundances across a range of bacterial taxa. We further show that depletion of SD sequences within ribosomal protein genes is correlated with organismal growth rates, supporting the hypothesis of strong selection against the presence of these sequences in coding regions and suggesting their association with translation efficiency in bacteria.
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spelling pubmed-51008452016-11-09 Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent Yang, Chuyue Hockenberry, Adam J. Jewett, Michael C. Amaral, Luís A. N. G3 (Bethesda) Investigations Efficient and accurate protein synthesis is crucial for organismal survival in competitive environments. Translation efficiency (the number of proteins translated from a single mRNA in a given time period) is the combined result of differential translation initiation, elongation, and termination rates. Previous research identified the Shine-Dalgarno (SD) sequence as a modulator of translation initiation in bacterial genes, while codon usage biases are frequently implicated as a primary determinant of elongation rate variation. Recent studies have suggested that SD sequences within coding sequences may negatively affect translation elongation speed, but this claim remains controversial. Here, we present a metric to quantify the prevalence of SD sequences in coding regions. We analyze hundreds of bacterial genomes and find that the coding sequences of highly expressed genes systematically contain fewer SD sequences than expected, yielding a robust correlation between the normalized occurrence of SD sites and protein abundances across a range of bacterial taxa. We further show that depletion of SD sequences within ribosomal protein genes is correlated with organismal growth rates, supporting the hypothesis of strong selection against the presence of these sequences in coding regions and suggesting their association with translation efficiency in bacteria. Genetics Society of America 2016-09-07 /pmc/articles/PMC5100845/ /pubmed/27605518 http://dx.doi.org/10.1534/g3.116.032227 Text en Copyright © 2016 Yang et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigations
Yang, Chuyue
Hockenberry, Adam J.
Jewett, Michael C.
Amaral, Luís A. N.
Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
title Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
title_full Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
title_fullStr Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
title_full_unstemmed Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
title_short Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
title_sort depletion of shine-dalgarno sequences within bacterial coding regions is expression dependent
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100845/
https://www.ncbi.nlm.nih.gov/pubmed/27605518
http://dx.doi.org/10.1534/g3.116.032227
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AT jewettmichaelc depletionofshinedalgarnosequenceswithinbacterialcodingregionsisexpressiondependent
AT amaralluisan depletionofshinedalgarnosequenceswithinbacterialcodingregionsisexpressiondependent