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

David S Milner; Jeremy G Wideman; Courtney W Stairs; Cory D Dunn; Thomas A Richards

doi:10.1371/journal.pbio.3001126

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

PLoS Biol. 2021 Apr 23;19(4):e3001126. doi: 10.1371/journal.pbio.3001126. eCollection 2021 Apr.

Authors

David S Milner¹, Jeremy G Wideman^{2

3}, Courtney W Stairs⁴, Cory D Dunn⁵, Thomas A Richards¹

Affiliations

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.

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Bacteria / genetics*
Base Sequence
DNA Restriction-Modification Enzymes / genetics*
DNA, Mitochondrial / analysis
DNA, Mitochondrial / genetics
Escherichia coli / genetics
Eukaryota / classification
Eukaryota / genetics*
Evolution, Molecular*
Gene Transfer, Horizontal
Genome, Mitochondrial / genetics
Mitochondria / genetics*
Organisms, Genetically Modified
Phylogeny
Repetitive Sequences, Nucleic Acid / genetics
Saccharomyces cerevisiae / genetics
Sequence Analysis, DNA

Substances

DNA Restriction-Modification Enzymes
DNA, Mitochondrial

Associated data

figshare/10.6084/m9.figshare.7352966
figshare/10.6084/m9.figshare.7314728
figshare/10.6084/m9.figshare.c.5336963

Grants and funding

C.D.D. is supported by the Sigrid Jusélius Foundation, the Academy of Finland (https://www.aka.fi, grant no. 331556), and the Jane and Aatos Erkko Foundation (https://jaes.fi). C.W.S is supported by a Vetenskaprådet starting grant from the Swedish Research Council (https://www.vr.se, grant no. 2020-05071). T.A.R. is supported by a Royal Society University Research Fellowship (https://royalsociety.org, grant no. UF130382) and additional funding through the European Molecular Biology Organisation Young Investigator Program (www.embo.org). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.