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A functional bacteria-derived restriction modification system in the mitochondrion of a heterotrophic protist
Authors:David S Milner  Jeremy G Wideman  Courtney W Stairs  Cory D Dunn  Thomas A Richards
Institution:1. Department of Zoology, University of Oxford, Oxford, United Kingdom;2. Biodesign Center for Mechanisms of Evolution, School of Life Sciences, Arizona State University, Tempe, Arizona, United States of America;3. Wissenschaftskolleg zu Berlin, Berlin, Germany;4. Department of Biology, Lund University, Lund, Sweden;5. Institute of Biotechnology, Helsinki Institute of Life Science, University of Helsinki, Helsinki, Finland;Fred Hutchinson Cancer Research Center, UNITED STATES
Abstract:The overarching trend in mitochondrial genome evolution is functional streamlining coupled with gene loss. Therefore, gene acquisition by mitochondria is considered to be exceedingly rare. Selfish elements in the form of self-splicing introns occur in many organellar genomes, but the wider diversity of selfish elements, and how they persist in the DNA of organelles, has not been explored. In the mitochondrial genome of a marine heterotrophic katablepharid protist, we identify a functional type II restriction modification (RM) system originating from a horizontal gene transfer (HGT) event involving bacteria related to flavobacteria. This RM system consists of an HpaII-like endonuclease and a cognate cytosine methyltransferase (CM). We demonstrate that these proteins are functional by heterologous expression in both bacterial and eukaryotic cells. These results suggest that a mitochondrion-encoded RM system can function as a toxin–antitoxin selfish element, and that such elements could be co-opted by eukaryotic genomes to drive biased organellar inheritance.

This study reveals that a functional type II restriction modification system of flavobacterial ancestry has been horizontally transferred into the mitochondrion of a marine protist and is capable of encoding potent function, perhaps allowing it to play a role in inter-organellar warfare or protection against further integration of foreign DNA.
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