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GENETICS
A bacterial group II intron favors retrotransposition into plasmid targets

Kenji Ichiyanagi ^*  , Arthur Beauregard ^*  , and Marlene Belfort ^*  ¶

^*Molecular Genetics Program, Wadsworth Center, New York State Department of Health, and School of Public Health, State University of New York, P.O. Box 22002, Albany, NY 12201-2002

Contributed by Marlene Belfort, October 15, 2003

Group II introns, widely believed to be the ancestors of nuclear pre-mRNA introns, are catalytic RNAs found in bacteria, archaea, and eukaryotes. They are mobile genetic elements that move via an RNA intermediate. They retrohome to intronless alleles and retrotranspose to ectopic sites, aided by an intron-encoded protein with reverse transcriptase, maturase, and endonuclease activities. Many group II introns identified in bacteria reside on plasmid genomes rather than bacterial chromosomes, implying that plasmids are havens for these retroelements. This study demonstrates that almost one-fourth of retrotransposition events of the Ll.LtrB intron in Lactococcus lactis are into the plasmid donor. This level is more than twice that predicted based on target size and plasmid copy number relative to the chromosome. In particular, the fraction of such plasmid targeting events was elevated to more than one-third of retrotransposition events by mutation of the intron-encoded endonuclease, a situation that may resemble most bacterial group II introns, which lack the endonuclease. Target-site sequences on the plasmid are more relaxed than those on the chromosome, likely accounting for preferred integration into plasmid replicons. Furthermore, the direction of integration relative to promoters and origins of replication is consistent with group II intron retrotransposition into single-stranded DNA at replication forks. This work provides mechanistic rationales for the prevalence of group II introns in natural plasmid populations and underscores that targeting to plasmids, which are themselves mobile elements, could promote intron spread.

K.I. and A.B. contributed equally to this work.

Present address: Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan.

^¶ To whom correspondence should be addressed. E-mail: belfort{at}wadsworth.org.

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