For Group II Introns, More Heat Means More Mobility
| Autor: | Alan M. Lambowitz, Eman Ghanem, Georg Mohr |
|---|---|
| Rok vydání: | 2010 |
| Předmět: |
DNA
Bacterial Genome evolution Spliceosome QH301-705.5 Molecular Sequence Data Retrotransposon RNA-binding protein Molecular Biology/Molecular Evolution Biology Molecular Biology/RNA Splicing Cyanobacteria General Biochemistry Genetics and Molecular Biology Molecular Biology/Bioinformatics Open Reading Frames 03 medical and health sciences 0302 clinical medicine Minor spliceosome Sequence Homology Nucleic Acid Biochemistry/RNA Structure Group I catalytic intron Biology (General) Gene 030304 developmental biology Genetics 0303 health sciences Base Sequence General Immunology and Microbiology General Neuroscience Intron RNA Group II intron Introns RNA splicing Synopsis Molecular Biology/RNA-Protein Interactions General Agricultural and Biological Sciences Genome Bacterial 030217 neurology & neurosurgery Research Article |
| Zdroj: | PLoS Biology PLoS Biology, Vol 8, Iss 6, p e1000392 (2010) PLoS Biology, Vol 8, Iss 6, p e1000391 (2010) |
| ISSN: | 1545-7885 |
| Popis: | Studies of mobile group II introns from a thermophilic cyanobacterium reveal how these introns proliferate within genomes and might explain the origin of introns and retroelements in higher organisms. Mobile group II introns, which are found in bacterial and organellar genomes, are site-specific retroelments hypothesized to be evolutionary ancestors of spliceosomal introns and retrotransposons in higher organisms. Most bacteria, however, contain no more than one or a few group II introns, making it unclear how introns could have proliferated to higher copy numbers in eukaryotic genomes. An exception is the thermophilic cyanobacterium Thermosynechococcus elongatus, which contains 28 closely related copies of a group II intron, constituting ∼1.3% of the genome. Here, by using a combination of bioinformatics and mobility assays at different temperatures, we identified mechanisms that contribute to the proliferation of T. elongatus group II introns. These mechanisms include divergence of DNA target specificity to avoid target site saturation; adaptation of some intron-encoded reverse transcriptases to splice and mobilize multiple degenerate introns that do not encode reverse transcriptases, leading to a common splicing apparatus; and preferential insertion within other mobile introns or insertion elements, which provide new unoccupied sites in expanding non-essential DNA regions. Additionally, unlike mesophilic group II introns, the thermophilic T. elongatus introns rely on elevated temperatures to help promote DNA strand separation, enabling access to a larger number of DNA target sites by base pairing of the intron RNA, with minimal constraint from the reverse transcriptase. Our results provide insight into group II intron proliferation mechanisms and show that higher temperatures, which are thought to have prevailed on Earth during the emergence of eukaryotes, favor intron proliferation by increasing the accessibility of DNA target sites. We also identify actively mobile thermophilic introns, which may be useful for structural studies, gene targeting in thermophiles, and as a source of thermostable reverse transcriptases. Author Summary Group 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. |
| Databáze: | OpenAIRE |
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