Very small mobile repeated elements in cyanobacterial genomes

Abstract

Mobile DNA elements play a major role in genome plasticity and other evolutionary processes, an insight gained primarily through the study of transposons and retrotransposons (generally ∼1000 nt or longer). These elements spawn smaller parasitic versions (generally >100 nt) that propagate through proteins encoded by the full elements. Highly repeated sequences smaller than 100 nt have been described, but they are either nonmobile or their origins are not known. We have surveyed the genome of the multicellular cyanobacterium, Nostoc punctiforme, and its relatives for small dispersed repeat (SDR) sequences and have identified eight families in the range of from 21 to 27 nucleotides. Three of the families (SDR4, SDR5, and SDR6), despite little sequence similarity, share a common predicted secondary structure, a conclusion supported by patterns of compensatory mutations. The SDR elements are found in a diverse set of contexts, often embedded within tandemly repeated heptameric sequences or within minitransposons. One element (SDR5) is found exclusively within instances of an octamer, HIP1, that is highly over-represented in the genomes of many cyanobacteria. Two elements (SDR1 and SDR4) often are found within copies of themselves, producing complex nested insertions. An analysis of SDR elements within cyanobacterial genomes indicate that they are essentially confined to a coherent subgroup. The evidence indicates that some of the SDR elements, probably working through RNA intermediates, have been mobile in recent evolutionary time, making them perhaps the smallest known mobile elements.[Supplemental material is available online at www.genome.org.] The mechanisms by which new copies of dispersed repeats are generated are well understood in some, but by no means, all cases. Transposon copies arise through DNA intermediates, catalyzed by transposases (Gueguen et al. 2005). Copies of retroposons (and degenerate retroposons, such as Alu sequences) are made through RNA intermediates, catalyzed by reverse transcriptase (Ostertag and Kazazian 2001). Minitransposons (also called MITEs), a category that may include the well-studied ERIC sequences (De Gregario et al. 2005), are thought to rely on transposases encoded outside of the mobile element (Siguier et al. 2006). The 8-nt highly iterated palindromic (HIP1) sequences observed in the genomes of many related cyanobacteria are thought not to be mobile but rather to form through mutation from pre-existing sequences (Robinson et al. 1997), The mechanisms by which small dispersed repeats are generated are otherwise unknown.The genomes of the cyanobacterium Nostoc punctiforme ATCC 29,133 and its relatives are unusual in that about 1.5% (∼7.5% of intergenic sequences) is taken up by tandem repeats at least 20 nt in length (Meeks et al. 2001; J. Elhai, T. Katayama, R. Narikawa, S. Okamoto, C. Friedland, R. Nayak, M. Ikeuchi, and M. Kanehisa, unpubl.). Repeating units of 7 nt (Mazel et al. 1990;Meeks et al. 2001) are by far the most common, with only a few of the possible families ...

Abundance and distribution of the highly iterated palindrome 1 (HIP1) among prokaryotes

“…This observation suggests that HIP1 predates SRD5, but, it could be also possible that SDR5 has a different sequence outside heterocystous cyanobacteria and has been overlooked by previous analysis. 5 This point clearly deserves further attention. Here we show that in some prokaryotic genomes there is a statistically significant difference in the number of copies of HIP1 between coding and non-coding DNA.…”

“…For instance, the phylogenetic distribution of HIP1 is larger than that of SRD5. SDR5 is confined only to heterocystous cyanobacteria 5 while HIP1 has a much wider distribution. This observation suggests that HIP1 predates SRD5, but, it could be also possible that SDR5 has a different sequence outside heterocystous cyanobacteria and has been overlooked by previous analysis.…”

“…5 The relationship between HIP1 and SDR5 is not understood, but it has been hypothesized that SDR5 could integrate into HIP1 through target-primed reverse transcription. 5 In this study we address the phylogenetic distribution of HIP1 among completely sequenced prokaryotic genomes, its frequency of occurrence among coding and non-coding regions, and its cooccurrence with DAM methylases and other proteins among cyanobacteria. Finally, we test the hypothesis that HIP1 could serve as a water-mark of horizontally transferred genes from cyanobacteria to other prokaryotic lineages.…”

“…3,4 More recent studies showed that one kind of repetitive element named Small Dispersed Repeat 5 (SDR5) is found interrupting HIP1 motifs between their third and fourth nucleotide in Nostoc punctiforme (i.e., 5'-GCG|ATCGC-3', where the vertical bar indicates the place of insertion of SDR5). 5 This repeat (SDR5) consist of 21 nucleotides that seems to fold into an stable secondary structure. 5 The relationship between HIP1 and SDR5 is not understood, but it has been hypothesized that SDR5 could integrate into HIP1 through target-primed reverse transcription.…”

“…5 This repeat (SDR5) consist of 21 nucleotides that seems to fold into an stable secondary structure. 5 The relationship between HIP1 and SDR5 is not understood, but it has been hypothesized that SDR5 could integrate into HIP1 through target-primed reverse transcription. 5 In this study we address the phylogenetic distribution of HIP1 among completely sequenced prokaryotic genomes, its frequency of occurrence among coding and non-coding regions, and its cooccurrence with DAM methylases and other proteins among cyanobacteria.…”