Evolutionary analysis of polyproline motifs in Escherichia coli reveals their regulatory role in translation

PLoS Comput Biol. 2018 Feb 1;14(2):e1005987. doi: 10.1371/journal.pcbi.1005987. eCollection 2018 Feb.

Abstract

Translation of consecutive prolines causes ribosome stalling, which is alleviated but cannot be fully compensated by the elongation factor P. However, the presence of polyproline motifs in about one third of the E. coli proteins underlines their potential functional importance, which remains largely unexplored. We conducted an evolutionary analysis of polyproline motifs in the proteomes of 43 E. coli strains and found evidence of evolutionary selection against translational stalling, which is especially pronounced in proteins with high translational efficiency. Against the overall trend of polyproline motif loss in evolution, we observed their enrichment in the vicinity of translational start sites, in the inter-domain regions of multi-domain proteins, and downstream of transmembrane helices. Our analysis demonstrates that the time gain caused by ribosome pausing at polyproline motifs might be advantageous in protein regions bracketing domains and transmembrane helices. Polyproline motifs might therefore be crucial for co-translational folding and membrane insertion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs*
  • Escherichia coli / metabolism*
  • Escherichia coli Proteins / metabolism
  • Evolution, Molecular
  • Peptide Chain Elongation, Translational*
  • Peptide Elongation Factors / metabolism
  • Peptides / chemistry*
  • Phylogeny
  • Protein Biosynthesis*
  • Protein Folding
  • Proteome / metabolism
  • Proteomics
  • Ribosomes / metabolism

Substances

  • Escherichia coli Proteins
  • Peptide Elongation Factors
  • Peptides
  • Proteome
  • factor EF-P
  • polyproline

Grants and funding

This work was supported by the DFG: Center for Integrated Protein Science Munich (CIPSM) (http://www.dfg.de/; Exc114/2 and TRR174/P09 to KJ, and LA 3658/1-1 to JL) and the China Scholarship Council (http://www.csc.edu.cn/; 201206740006 to FQ). This work was supported by the German Research Foundation (DFG) and the Technical University of Munich (TUM) in the framework of the Open Access Publishing Program. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.