Survey of chimeric IStron elements in bacterial genomes: multiple molecular symbioses between group I intron ribozymes and DNA transposons.

Nicolas J Tourasse,Anne-Brit Kolstø,Fredrik B Stabell

doi:10.1093/nar/gku939

Abstract

IStrons are chimeric genetic elements composed of a group I intron associated with an insertion sequence (IS). The group I intron is a catalytic RNA providing the IStron with self-splicing ability, which renders IStron insertions harmless to the host genome. The IS element is a DNA transposon conferring mobility, and thus allowing the IStron to spread in genomes. IStrons are therefore a striking example of a molecular symbiosis between unrelated genetic elements endowed with different functions. In this study, we have conducted the first comprehensive survey of IStrons in sequenced genomes that provides insights into the distribution, diversity, origin and evolution of IStrons. We show that IStrons have a restricted phylogenetic distribution limited to two bacterial phyla, the Firmicutes and the Fusobacteria. Nevertheless, diverse IStrons representing two major groups targeting different insertion site motifs were identified. This taken with the finding that while the intron components of all IStrons belong to the same structural class, they are fused to different IS families, indicates that multiple intron–IS symbioses have occurred during evolution. In addition, introns and IS elements related to those that were at the origin of IStrons were also identified.

Highlights

Over the past decades it has been well recognized that mobile genetic elements have played a major role in genomic evolution
The protein sequences of the open reading frames (ORFs) encoded by all insertion sequence (IS) elements listed in ISfinder were searched against GenBank to retrieve these proteins and their homologues
In Bacteria IStrons were present in 117 strains from 18 species that belong to only two different phyla, the Firmicutes and the Fusobacteria

Summary

Introduction

Over the past decades it has been well recognized that mobile genetic elements have played a major role in genomic evolution. Insertion sequences (ISs in prokaryotes; class II DNA transposons in eukaryotes) are among the best known and widespread mobile elements. They are relatively simple and compact transposable DNA elements. A typical IS transposon is a piece of sequence ranging from 700 to 2500 bp (in prokaryotes) or >5000 bp (in eukaryotes) in length, encoding one or two open reading frames (ORFs), surrounded by 5 and 3 flanking sequences (often ending with terminal inverted repeats (IRs); for reviews see [6,7,8,9,10,11]). The ORFs encode transposases or other DNA recombinases such as tyrosine or serine recombinases or resolvases that are responsible for IS mobility within and between genomes, and they are usually highly specific to their cognate transposons. A few transposition mechanisms have been characterized, while the mechanisms of many IS elements are yet to be deciphered (for reviews see [6,8,11,12,13,14,15])

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Conclusion