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

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.

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“…However, in these mobile elements, a transposase is located within the loop of the large hairpin. A recent genome survey found that IStrons were restricted to a few members of the Firmicutes and Fusobacteria (Tourasse et al, 2014 ). Unlike group I introns, IStrons invade many types of protein-coding genes and are often found without some, or all, of the IS components, making them appear more like a MITE.…”

“…The IS200/IS605 family of IS elements are unique among known IS elements in that they encode a HUH endonuclease that recognizes a terminal imperfect palindrome and then transposes it into a single strand of genomic DNA (He et al, 2013 ). They are also unique in that they have been found in IStrons (see Tourasse et al, 2014 , and references therein). This IS family also has the potential to transform or decay into a unique MITE-like structures called palindrome-associated transition elements (PATEs) (Dyall-Smith et al, 2011 ; Siguier et al, 2014 ).…”

“…The ribozymal activity was found to be temperature dependent, promoting motility under higher temperatures and thus the intron may function in a regulatory role for flagellin gene expression under lower temperatures (Hayakawa and Ishizuka, 2012 ). The only other reported examples group I introns are the IStrons found in a few Firmicutes and Fusobacteria (Tourasse et al, 2014 ). IStrons have been shown to have alternative splicing sites, which could lead to different protein variants (Hasselmayer et al, 2004 ).…”

“…IStrons have been shown to have alternative splicing sites, which could lead to different protein variants (Hasselmayer et al, 2004 ). Some of these IStrons have been found without transposases (Tourasse et al, 2014 ). However, we did not find any reports of MITE-like sequences similar to IS elements within IStrons in these genomes.…”

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“…Even for lytic viruses, data are accumulating on frequent integration into the host genomes, even if this process is spurious with respect to virus reproduction (Chiba et al 2011; Koonin 2010; Liu et al 2010). A striking example of fusion between distinct parasitic replicators are the IStrons which are hybrids between Group I self-splicing introns and insertion sequences, and combine properties of introns and DNA transposons (Tourasse et al 2014). Similarly, large DNA viruses often harbor self-splicing introns and serve as vehicles for their dissemination (Edgell et al 2011; Yoosuf et al 2012).…”