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

Milner, David S ; Wideman, Jeremy G ; Stairs, Courtney W LU orcid ; Dunn, Cory D and Richards, Thomas A (2021) In PLoS Biology 19(4).
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... (More)

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 mitochondrial-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.

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author
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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
PLoS Biology
volume
19
issue
4
article number
e3001126
pages
19 pages
publisher
Public Library of Science (PLoS)
external identifiers
  • pmid:33891594
  • scopus:85104829265
ISSN
1545-7885
DOI
10.1371/journal.pbio.3001126
language
English
LU publication?
yes
id
3e723662-543d-48e0-89d0-64edb33809d9
date added to LUP
2021-04-27 18:55:28
date last changed
2024-04-20 05:32:51
@article{3e723662-543d-48e0-89d0-64edb33809d9,
  abstract     = {{<p>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 mitochondrial-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.</p>}},
  author       = {{Milner, David S and Wideman, Jeremy G and Stairs, Courtney W and Dunn, Cory D and Richards, Thomas A}},
  issn         = {{1545-7885}},
  language     = {{eng}},
  month        = {{04}},
  number       = {{4}},
  publisher    = {{Public Library of Science (PLoS)}},
  series       = {{PLoS Biology}},
  title        = {{A functional bacteria-derived restriction modification system in the mitochondrion of a heterotrophic protist}},
  url          = {{http://dx.doi.org/10.1371/journal.pbio.3001126}},
  doi          = {{10.1371/journal.pbio.3001126}},
  volume       = {{19}},
  year         = {{2021}},
}