Abstract

Four group II introns were found in an unusually intron-rich dnaN gene (encoding the beta subunit of DNA polymerase III) of the cyanobacterium Trichodesmium erythraeum, and they have strong similarities to two introns of the RIR gene (encoding ribonucleotide reductase) of the same organism. Of these six introns, only the RIR-3 intron encodes a maturase protein and showed efficient RNA splicing when expressed in Escherichia coli cells. The other five introns do not encode a maturase protein and did not show RNA splicing in E. coli. But these maturase-less introns showed efficient RNA splicing when the RIR-3 intron-encoded maturase protein was co-expressed from a freestanding gene in the same cell. These findings demonstrated that an intron-encoded protein could function as a general maturase for multiple introns of different genes. Major implications may include an intron-mediated co-regulation of the different genes and a resemblance of the evolutionary origin of spliceosomal introns.

Highlights

  • Group II introns are mobile genetic elements and presumed evolutionary progenitors of nuclear spliceosomal introns [1, 2]

  • We report an unusual case of four maturase-less group II introns in a conserved bacterial protein gene, which is the largest number of introns known in a bacterial gene

  • Identification and Sequence Analysis of dnaN Gene and Its Introns—The recent findings of group II introns in an RIR gene [16] prompted us to find similar introns in related genes in the nearly complete genome sequence of the oceanic N2-fixing cyanobacterium T. erythraeum strain IMS101, which had been determined at the United States Department of Energy Joint Genome Institute

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Summary

ACCELERATED PUBLICATION

An Intron-encoded Protein Assists RNA Splicing of Multiple Similar Introns of Different Bacterial Genes*. Four group II introns were found in an unusually intron-rich dnaN gene (encoding the ␤ subunit of DNA polymerase III) of the cyanobacterium Trichodesmium erythraeum, and they have strong similarities to two introns of the RIR gene (encoding ribonucleotide reductase) of the same organism Of these six introns, only the RIR-3 intron encodes a maturase protein and showed efficient RNA splicing when expressed in Escherichia coli cells. We report an unusual case of four maturase-less group II introns in a conserved bacterial protein gene, which is the largest number of introns known in a bacterial gene These maturase-less introns could do RNA splicing in Escherichia coli when assisted by a maturase protein encoded. This demonstrated for the first time that an intron-encoded protein could function as a general maturase for multiple introns of different genes, which has interesting implications on intron evolution and on possible roles of intron in coordinating gene expression

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