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. 2005;6(3):R25.
doi: 10.1186/gb-2005-6-3-r25. Epub 2005 Feb 15.

Transcriptional slippage in bacteria: distribution in sequenced genomes and utilization in IS element gene expression

Pavel V Baranov  1 , Andrew W Hammer, Jiadong Zhou, Raymond F Gesteland, John F Atkins
Affiliations

Transcriptional slippage in bacteria: distribution in sequenced genomes and utilization in IS element gene expression

Pavel V Baranov et al. Genome Biol. 2005.

Abstract

Background: Transcription slippage occurs on certain patterns of repeat mononucleotides, resulting in synthesis of a heterogeneous population of mRNAs. Individual mRNA molecules within this population differ in the number of nucleotides they contain that are not specified by the template. When transcriptional slippage occurs in a coding sequence, translation of the resulting mRNAs yields more than one protein product. Except where the products of the resulting mRNAs have distinct functions, transcription slippage occurring in a coding region is expected to be disadvantageous. This probably leads to selection against most slippage-prone sequences in coding regions.

Results: To find a length at which such selection is evident, we analyzed the distribution of repetitive runs of A and T of different lengths in 108 bacterial genomes. This length varies significantly among different bacteria, but in a large proportion of available genomes corresponds to nine nucleotides. Comparative sequence analysis of these genomes was used to identify occurrences of 9A and 9T transcriptional slippage-prone sequences used for gene expression.

Conclusions: IS element genes are the largest group found to exploit this phenomenon. A number of genes with disrupted open reading frames (ORFs) have slippage-prone sequences at which transcriptional slippage would result in uninterrupted ORF restoration at the mRNA level. The ability of such genes to encode functional full-length protein products brings into question their annotation as pseudogenes and in these cases is pertinent to the significance of the term 'authentic frameshift' frequently assigned to such genes.

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Figures

Figure 1
Figure 1
A scheme for the nonlinear expression of Thermus thermophilus dnaX via transcriptional slippage. Transcription of dnaX results in synthesis of a population of mRNAs in which the sequence 3' of the slippery AAAAAAAAA is framed in different molecules in all three reading frames relative to sequence 5' of the slippery motif.
Figure 2
Figure 2
Analysis of the distribution of runs of As and Ts in selected genomes. Run length is indicated on the x-axis; the ratio of pattern occurrence on the y-axis. (a) Ratio of occurrences in coding regions and in entire genomic sequences. (b) Ratio of occurrences of A runs in real genomes and average occurrence in 1,000 randomized genomes. Biases preserved during the randomization procedure are indicated above each pair of graphs. Accession numbers are as follows: NC_000913 E. coli K12; NC_000915 Helicobacter pylori; NC_000963 Rickettsia prowazekii; NC_001318 Borrelia burgdorferi; NC_002163 Campylobacter jejuni; NC_003450 Corynebacterium glutamicum; NC_003364 Pseudomonas aeruginosa; NC_004344 Wigglesworthia glossinidia.
Figure 3
Figure 3
Scheme for functional analysis of slippery patterns in coding sequences.
Figure 4
Figure 4
Different types of ORF organization for genes sharing sequence similarities.
Figure 5
Figure 5
Codon alignments of DNA and mRNA sequences of orthologous genes from two different strains of E. coli. In the DNA, an A causing a frameshift mutation is underlined. In the mRNA, a tandem A inserted by transcriptional slippage which results in ORF restoration is underlined.
Figure 6
Figure 6
Alignment of a portion of Deinococcus radiodurans IS elements containing a run of nine or eight As. Universally conserved residues are in bold, runs of As are in red. The alignment was built using Clustal [54].
Figure 7
Figure 7
A model of transcriptional slippage.
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