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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Main Authors: Chuyue Yang, Adam J. Hockenberry, Michael C. Jewett, Luís A. N. Amaral
Format: Article
Language:English
Published: Oxford University Press 2016-11-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.116.032227
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spelling doaj-1e9934723e52437da4c09871883226ac2021-07-02T04:18:43ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362016-11-016113467347410.1534/g3.116.0322273Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression DependentChuyue YangAdam J. HockenberryMichael C. JewettLuís A. N. AmaralEfficient 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.http://g3journal.org/lookup/doi/10.1534/g3.116.032227translation initiationgene expressiongrowth regulation
collection DOAJ
language English
format Article
sources DOAJ
author Chuyue Yang
Adam J. Hockenberry
Michael C. Jewett
Luís A. N. Amaral
spellingShingle Chuyue Yang
Adam J. Hockenberry
Michael C. Jewett
Luís A. N. Amaral
Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
G3: Genes, Genomes, Genetics
translation initiation
gene expression
growth regulation
author_facet Chuyue Yang
Adam J. Hockenberry
Michael C. Jewett
Luís A. N. Amaral
author_sort Chuyue Yang
title 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_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_sort depletion of shine-dalgarno sequences within bacterial coding regions is expression dependent
publisher Oxford University Press
series G3: Genes, Genomes, Genetics
issn 2160-1836
publishDate 2016-11-01
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.
topic translation initiation
gene expression
growth regulation
url http://g3journal.org/lookup/doi/10.1534/g3.116.032227
work_keys_str_mv AT chuyueyang depletionofshinedalgarnosequenceswithinbacterialcodingregionsisexpressiondependent
AT adamjhockenberry depletionofshinedalgarnosequenceswithinbacterialcodingregionsisexpressiondependent
AT michaelcjewett depletionofshinedalgarnosequenceswithinbacterialcodingregionsisexpressiondependent
AT luisanamaral depletionofshinedalgarnosequenceswithinbacterialcodingregionsisexpressiondependent
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