YraN is a helicase-associated nuclease fostering extended recombination events by natural transformation
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Natural transformation is a widespread molecular pathway of horizontal gene transfer involving the uptake and recombination of exogenous DNA. Exogenous DNA follows a pathway involving genes sequentially required for its capture, internalization, protection, and recombination with the chromosome. Most of these genes were identified through the isolation of transformation-defective mutants and/or based on their expression preceding natural transformation. Yet, genes required for key steps of the pathway remain elusive. We sought to identify any missing component by comparing Tn-seq data obtained in two distantly-related transformable diderm species, the human pathogen Legionella pneumophila and the cyanobacterium Synechococcus elongatus . We identified yraN , a widespread and highly conserved gene of unknown function required for natural transformation. We provide evidence that YraN is a nuclease associated with the ComM helicase, which cooperate to process the D-loop formed by the invasion of the transforming DNA in the chromosomal DNA strands. We propose a model in which cleavage of the displaced strand by YraN can promote the recombination of transforming DNA, leading to extended recombination events. The identification of this YraN/ComM nuclease/helicase system supports the hypothesis that bacteria possess a conserved pathway for the transport and recombination of exogenous DNA.
Significance
Many bacteria use a dedicated pathway to internalize and integrate extracellular DNA into their chromosome. This allows them to naturally acquire genes, or gene variants, that can confer them new traits, hence the term of natural transformation. Although reported nearly a century ago by Frederick Griffith, several aspects of the mechanism of natural transformation remain elusive. Specifically, it is not clear whether or not all the conserved molecular players of the pathway have been identified. We queried two distinct bacterial species for any gene that would be required for natural transformation. We confirmed all core players of the pathway, but also uncovered a highly conserved one, YraN. We provide evidence that YraN is an endonuclease, which in association with the ComM helicase, promotes the efficient integration of the extracellular DNA in the bacterial chromosome.
