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PLoS genetics
Dec, 2014;10 (12): e1004853.

Interaction between conjugative and retrotransposable elements in horizontal gene transfer.

Olga Novikova, Dorie Smith, Ingrid Hahn, Arthur Beauregard, Marlene Belfort
Author Information
  1. Olga Novikova: Department of Biological Sciences and RNA Institute, University at Albany, Albany, New York, United States of America.
  2. Dorie Smith: Department of Biological Sciences and RNA Institute, University at Albany, Albany, New York, United States of America.
  3. Ingrid Hahn: Department of Biomedical Sciences, University at Albany, Wadsworth Center, NYS Department of Health, Albany, New York, United States of America.
  4. Arthur Beauregard: Department of Biomedical Sciences, University at Albany, Wadsworth Center, NYS Department of Health, Albany, New York, United States of America.
  5. Marlene Belfort: Department of Biological Sciences and RNA Institute, University at Albany, Albany, New York, United States of America.
PMID: 25474706 DOI: 10.1371/journal.pgen.1004853

Abstract

Mobile genetic elements either encode their own mobilization machineries or hijack them from other mobile elements. Multiple classes of mobile elements often coexist within genomes and it is unclear whether they have the capacity to functionally interact and even collaborate. We investigate the possibility that molecular machineries of disparate mobile elements may functionally interact, using the example of a retrotransposon, in the form of a mobile group II intron, found on a conjugative plasmid pRS01 in Lactococcus lactis. This intron resides within the pRS01 ltrB gene encoding relaxase, the enzyme required for nicking the transfer origin (oriT) for conjugal transmission of the plasmid into a recipient cell. Here, we show that relaxase stimulates both the frequency and diversity of retrotransposition events using a retromobility indicator gene (RIG), and by developing a high-throughput genomic retrotransposition detection system called RIG-Seq. We demonstrate that LtrB relaxase not only nicks ssDNA of its cognate oriT in a sequence- and strand-specific manner, but also possesses weak off-target activity. Together, the data support a model in which the two different mobile elements, one using an RNA-based mechanism, the other using DNA-based transfer, do functionally interact. Intron splicing facilitates relaxase expression required for conjugation, whereas relaxase introduces spurious nicks in recipient DNA that stimulate both the frequency of intron mobility and the density of events. We hypothesize that this functional interaction between the mobile elements would promote horizontal conjugal gene transfer while stimulating intron dissemination in the donor and recipient cells.

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Grants

  1. GM44844/NIGMS NIH HHS
  2. R37 GM039422/NIGMS NIH HHS
  3. GM39422/NIGMS NIH HHS
  4. R01 GM039422/NIGMS NIH HHS
  5. R01 GM044844/NIGMS NIH HHS

MeSH Term

Base Sequence
Conjugation, Genetic
DNA, Single-Stranded
Endoribonucleases
Epistasis, Genetic
Gene Transfer, Horizontal
Introns
Lactococcus lactis
Organisms, Genetically Modified
RNA Splicing
Retroelements

Chemicals

DNA, Single-Stranded
Retroelements
Endoribonucleases
Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't
Article has an altmetric score of 4

Word Cloud

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