A functional bacteria-derived restriction modification system in the mitochondrion of a heterotrophic protist.

David S Milner,Thomas A Richards,Jeremy G Wideman,Courtney W Stairs,Cory D Dunn,Harmit S Malik

doi:10.1371/journal.pbio.3001126

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.

Highlights

Endosymbiosis, the localisation and functional integration of one cell within another [1,2,3], can lead to the evolution of specialised organellar compartments responsible for a range of cellular and biochemical functions [4]
The Kat-HpaII restriction modification (RM) system is flanked by near-identical (152/155-bp) sequences that may reflect the recent integration of this selfish element into the katablepharid mitochondrial DNA (mtDNA)
We identified a number of eukaryotic transcripts from geographically diverse marine sampling sites with high percentage nucleotide identity to the kat-HpaII, kat-HpaII-cytosine methyltransferase (CM), and kat-MutH-like endonuclease (MutH)-CM genes (S1 Data), thereby demonstrating that this selfish genetic element is expressed from the katablepharid mitochondrial genome

Summary

Introduction

Endosymbiosis, the localisation and functional integration of one cell within another [1,2,3], can lead to the evolution of specialised organellar compartments responsible for a range of cellular and biochemical functions [4]. While sequencing initiatives have demonstrated that mitochondrial gene content can vary extensively, their evolution in every eukaryotic lineage is typified by both functional and genomic reduction [7,8]. Rare gene replacements and novel gene acquisitions into mitochondrial genomes have been identified [9,10], involving plant-to-plant gene transfers [11,12,13,14], with plants susceptible to the transfer of entire organelles, and their genomes, from one cell to another [15,16,17]. Mitochondrial group I and II self-splicing introns demonstrate a pattern

Methods

Results

Conclusion