Structural Organization and Functional Properties of Miniature DNA Insertion Sequences in Yersiniae

Abstract

YPALs (Yersinia palindromic sequences) are miniature DNA insertions scattered along the chromosomes of yersiniae. The spread of these intergenic repeats likely occurred via transposition, as suggested by the presence of target site duplications at their termini and the identification of syntenic chromosomal regions which differ in the presence/absence of YPAL DNA among Yersinia strains. YPALs tend to be inserted closely downstream from the stop codon of flanking genes, and many YPAL targets overlap rho-independent transcriptional terminator-like sequences. This peculiar pattern of insertion supports the hypothesis that most of these repeats are cotranscribed with upstream sequences into mRNAs. YPAL RNAs fold into stable hairpins which may modulate mRNA decay. Accordingly, we found that YPAL-positive transcripts accumulate in Yersinia enterocolitica cells at significantly higher levels than homologous transcripts lacking YPAL sequences in their 3 untranslated region.Bacterial insertion sequences (ISs) are mobile genetic elements ranging in size from 800 to 2,500 bp which are widely distributed among bacteria (21, 5). Typically, ISs encode a transposase which mediates their movement and feature terminal inverted repeats (TIRs) 10 to 50 bp long, which serve as recognition sites for the transposase. Most ISs generate short direct repeats (target site duplications [TSDs]) at the point of insertion. For each element, the length of the TSD is fixed and ranges from 2 to 13 bp. Differences in the structural organization, coding capacity, and transposition properties make it possible to sort ISs into approximately 20 major subfamilies (21).In recent years, it has emerged that small IS-like sequences called MITEs (for miniature transposable elements) may be a relevant genome component in several eukaryotic species (16,20). These elements characteristically measure 150 to 400 bp, carry long TIRs, and are flanked by TSDs of variable lengths. MITEs likely represent deletion derivatives of longer, autonomous ISs, which have been mobilized by tranposases encoded by partly related mobile donor elements (20). Several MITE families have also been identified in archaeabacteria (5). Three families of MITEs have been described for eubacteria. RUP (repeat unit of pneumococcus) elements are spread in ϳ100 copies in the genome of the Streptococcus pneumoniae 4 strain, and it has been proposed that their mobilization is mediated by the IS630-Spn1 element (24). NEMIS (Neisseria miniature insertion sequences) are 108-to 158-bp-long repeats which make up ϳ2% of the Neisseria meningitidis genome. In contrast to RUP elements, which are mostly interspersed with other repeated DNA sequences, NEMIS sequences are frequently located next to Neisseria genes and are transcribed into mRNAs. Hairpins formed by the pairing of NEMIS TIRs are targeted by RNase III, and this interaction regulates sets of N. meningitidis genes at the posttranscriptional level (12, 13).A different type of eubacterial MITE is represented by ERIC (enterobacterial repetitive i...

Enterobacterial Small Mobile Sequences Carry Open Reading Frames and are Found Intragenically–-Evolutionary Implications for Formation of New Peptides

“…Another class of mobile repeat units of approximately 167-bp, Yersinia palindromic sequences (YPAL) and termed RU-2 in this study, was recently reported to be present in Yersinia species (De Gregorio et al 2006). Independently, we also detected this class of repeat unit, which has an approximate 168-bp chain length and is found in 60 different intergenic regions of the Yersinia pestis chromosome.…”

“…While scanning genomic sequences in Yersinia species for the E. coli non-coding RNA gene itsR (Vogel et al 2004), a 168-bp sequence was found which is related to a previously described 167-bp repeat (De Gregorio et al 2006). The nucleotide sequence of a representative repeat element from the Y. pestis CO92 genome (termed RU-2) and its location in the genome are shown in Table 1b.…”

“…Repeat sequences in intergenic regions of enterobacterial genomes have been proposed to regulate mRNAs encoded by genes that are upstream of the repeat element (De Gregorio et al 2005; De Gregorio et al 2006). Interestingly, intergenic repeats elements similar to the RUs of enterobacterial, called CIR motifs, have also been found in Caulobacter and these elements may be associated with DNA methylation sites (Chen and Shapiro, 2003).…”

“…These fascinating mobile sequences are part of a class of bacterial small repeat elements that have close similarities to miniature inverted-repeat transposable elements (MITE) of eukaryotes and archaea microorganisms (Bureau and Wessler, 1992; Redder et al 2001) in terms of having small polynucleotide chain lengths and terminal inverted repeats. The enterobacterial repeat elements also display stable stem loop secondary structures, TA dinucleotides at their terminal ends and TA duplications at target site insertions (De Gregorio et al 2006; Wilson and Sharp, 2006). Neither bacterial, archaeon, or eukaryotic mobile elements encode proteins and thus are considered non-autonomous transposable elements.…”

Stenotrophomonas maltophilia genomes: A start-up comparison

“…All strains were routinely grown in brain heart infusion at 37 1C, except for the environmental strains (LMG959, LMG10871, LMG10879, LMG11104, and LMG11108) which were grown at 30 1C. Genomic DNA was extracted as described (De Gregorio et al, 2006). PCR amplifications.…”