Abstract
Author SummaryGroup II introns are bacterial mobile elements thought to be ancestors of introns and retroelements in higher organisms. They comprise a catalytically active intron RNA and an intron-encoded reverse transcriptase, which promotes splicing of the intron from precursor RNA and integration of the excised intron into new genomic sites. While most bacteria have small numbers of group II introns, in the thermophilic cyanobacterium Thermosynechococcus elongatus, a single intron has proliferated and constitutes 1.3% of the genome. Here, we investigated how the T. elongatus introns proliferated to such high copy numbers. We found divergence of DNA target specificity, evolution of reverse transcriptases that splice and mobilize multiple degenerate introns, and preferential insertion into other mobile introns or insertion elements, which provide new integration sites in non-essential regions of the genome. Further, unlike mesophilic group II introns, the thermophilic T. elongatus introns rely on higher temperatures to help promote DNA strand separation, facilitating access to DNA target sites. We speculate how these mechanisms, including elevated temperature, might have contributed to intron proliferation in early eukaryotes. We also identify actively mobile thermophilic introns, which may be useful for structural studies and biotechnological applications.
Highlights
Mobile group II introns are bacterial and organellar retrotransposons that are hypothesized to be ancestors or closely related to ancestors of spliceosomal introns and retrotransposons in higher organisms
Unlike mesophilic group II introns, the thermophilic T. elongatus introns rely on higher temperatures to help promote DNA strand separation, facilitating access to DNA target sites
Our results provide insight into how group II introns proliferate within genomes; show how higher temperatures, which are thought to have prevailed on Earth during the emergence of eukaryotes, can contribute to this process; and identify actively mobile thermophilic group II introns, which may be useful for structural studies and biotechnological applications
Summary
Mobile group II introns are bacterial and organellar retrotransposons that are hypothesized to be ancestors or closely related to ancestors of spliceosomal introns and retrotransposons in higher organisms (reviewed in [1,2]) They consist of a catalytically active intron RNA (‘‘ribozyme’’) and an intron-encoded protein (IEP), which has reverse transcriptase (RT) activity. For mobile group II introns, the IEP assists splicing by stabilizing the catalytically active RNA structure (‘‘maturase activity’’) and remains bound to the excised intron lariat RNA in a RNP (ribonucleoprotein particle) [6,7,8] The latter promotes intron mobility by a mechanism that involves reverse splicing of the intron RNA directly into a DNA strand, reverse transcription of the inserted intron RNA by the IEP, and integration of the resulting intron cDNA into the genome by host enzymes [9,10,11,12,13]. This mechanism is used by group II introns both to retrohome into specific DNA target sites at high frequency and to retrotranspose into ectopic sites that resemble the retrohoming site at low frequency, and ancestral mobile group II introns may have used the same mechanism to invade and proliferate within the nuclear genomes of early eukaryotes, before evolving into spliceosomal introns, snRNAs, and non-LTR-retrotransposons [1,2]
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