Distribution and diversity of ribosome binding sites in prokaryotic genomes.

Madhusudan Choudhary,Hyuk Cho,Damilola Omotajo,Travis Tate

doi:10.1186/s12864-015-1808-6

Abstract

BackgroundProkaryotic translation initiation involves the proper docking, anchoring, and accommodation of mRNA to the 30S ribosomal subunit. Three initiation factors (IF1, IF2, and IF3) and some ribosomal proteins mediate the assembly and activation of the translation initiation complex. Although the interaction between Shine-Dalgarno (SD) sequence and its complementary sequence in the 16S rRNA is important in initiation, some genes lacking an SD ribosome binding site (RBS) are still well expressed. The objective of this study is to examine the pattern of distribution and diversity of RBS in fully sequenced bacterial genomes. The following three hypotheses were tested: SD motifs are prevalent in bacterial genomes; all previously identified SD motifs are uniformly distributed across prokaryotes; and genes with specific cluster of orthologous gene (COG) functions differ in their use of SD motifs.ResultsData for 2,458 bacterial genomes, previously generated by Prodigal (PROkaryotic DYnamic programming Gene-finding ALgorithm) and currently available at the National Center for Biotechnology Information (NCBI), were analyzed. Of the total genes examined, ~77.0 % use an SD RBS, while ~23.0 % have no RBS. Majority of the genes with the most common SD motifs are distributed in a manner that is representative of their abundance for each COG functional category, while motifs 13 (5′-GGA-3′/5′-GAG-3′/5′-AGG-3′) and 27 (5′-AGGAGG-3′) appear to be predominantly used by genes for information storage and processing, and translation and ribosome biogenesis, respectively.ConclusionThese findings suggest that an SD sequence is not obligatory for translation initiation; instead, other signals, such as the RBS spacer, may have an overarching influence on translation of mRNAs. Subsequent analyses of the 5′ secondary structure of these mRNAs may provide further insight into the translation initiation mechanism.

Highlights

Prokaryotic translation initiation involves the proper docking, anchoring, and accommodation of mRNA to the 30S ribosomal subunit
It has been reported that the majority of the genes from archaebacterial species encode leaderless mRNAs, lacking ribosome binding site (RBS) motifs [11]; our result showed that 34 eubacterial genomes and 29 archaeal genomes contain genes that lack an RBS
We have studied the distribution of ribosome binding sites in 2458 completely sequenced prokaryotic genomes, in order to elucidate the possible impact of the presence and variation of RBS in translation initiation process

Summary

Introduction

Prokaryotic translation initiation involves the proper docking, anchoring, and accommodation of mRNA to the 30S ribosomal subunit. There are several potential initiation sites in an mRNA competing for a limited number of 30S subunits It has Omotajo et al BMC Genomics (2015) 16:604 been proposed that there is a purine-rich sequence similar to 5′-GGAGG-3′, the Shine Dalgarno (SD) sequence, located ~5–10 nucleotides upstream of the start codon in the mRNA [5]. In several cases (like in cyanobacteria), AT-rich motifs, instead of an SD sequence, are found upstream It is unknown whether these are genuine RBS motifs, a previous study has suggested that the ribosomal protein S1 binds to these AT-rich regions and unfolds the leader sequence of mRNA to make the start codon readily accessible [13]. In contrast to prokaryotic mRNAs, all eukaryotic mRNAs are leaderless and utilize a different translation initiation mechanism, where a translation initiation signal, the Kozak sequence [14], is embedded around the start codon

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