Depletion of Shine-Dalgarno sequences within bacterial coding regions is expression dependent

Chuyue Yang, Adam J. Hockenberry, Michael C. Jewett*, Luís A.N. Amaralv

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

14 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)3467-3474
Number of pages8
JournalG3: Genes, Genomes, Genetics
Volume6
Issue number11
DOIs
StatePublished - 2016

Funding

The authors would like to thank Sophia Liu for technical assistance related to data acquisition and helpful comments regarding the manuscript. C.Y. was supported by Northwestern University Undergraduate Research Programs (209WCASSUM133484; 342SUMMER155728). A.J.H. was supported by the National Institutes of Health training grant in Cellular and Molecular Basis of Disease (2-T32GM008061-31) and the Northwestern University Presidential Fellowship. M.C.J. was supported by the National Science Foundation (DMR-1108350; MCB-1413563), the David and Lucile Packard Foundation (2011-37152), and the Camille Dreyfus Teacher Scholar Award.

Keywords

  • Gene expression
  • Growth regulation
  • Translation initiation

ASJC Scopus subject areas

  • Molecular Biology
  • Genetics
  • Genetics(clinical)

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