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Bacterial N4-methylcytosine as an epigenetic mark in eukaryotic DNA

Author

Listed:
  • Fernando Rodriguez

    (Marine Biological Laboratory)

  • Irina A. Yushenova

    (Marine Biological Laboratory)

  • Daniel DiCorpo

    (Marine Biological Laboratory
    Boston University School of Public Health)

  • Irina R. Arkhipova

    (Marine Biological Laboratory)

Abstract

DNA modifications are used to regulate gene expression and defend against invading genetic elements. In eukaryotes, modifications predominantly involve C5-methylcytosine (5mC) and occasionally N6-methyladenine (6mA), while bacteria frequently use N4-methylcytosine (4mC) in addition to 5mC and 6mA. Here we report that 4mC can serve as an epigenetic mark in eukaryotes. Bdelloid rotifers, tiny freshwater invertebrates with transposon-poor genomes rich in foreign genes, lack canonical eukaryotic C5-methyltransferases for 5mC addition, but encode an amino-methyltransferase, N4CMT, captured from bacteria >60 Mya. N4CMT deposits 4mC at active transposons and certain tandem repeats, and fusion to a chromodomain shapes its “histone-read-DNA-write” architecture recognizing silent chromatin marks. Furthermore, amplification of SETDB1 H3K9me3 histone methyltransferases yields variants preferentially binding 4mC-DNA, suggesting “DNA-read-histone-write” partnership to maintain chromatin-based silencing. Our results show how non-native DNA methyl groups can reshape epigenetic systems to silence transposons and demonstrate the potential of horizontal gene transfer to drive regulatory innovation in eukaryotes.

Suggested Citation

  • Fernando Rodriguez & Irina A. Yushenova & Daniel DiCorpo & Irina R. Arkhipova, 2022. "Bacterial N4-methylcytosine as an epigenetic mark in eukaryotic DNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28471-w
    DOI: 10.1038/s41467-022-28471-w
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    1. Reuben W. Nowell & Fernando Rodriguez & Bette J. Hecox-Lea & David B. Mark Welch & Irina R. Arkhipova & Timothy G. Barraclough & Christopher G. Wilson, 2024. "Bdelloid rotifers deploy horizontally acquired biosynthetic genes against a fungal pathogen," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Emilien Nicolas & Paul Simion & Marc Guérineau & Matthieu Terwagne & Mathilde Colinet & Julie Virgo & Maxime Lingurski & Anaïs Boutsen & Marc Dieu & Bernard Hallet & Karine Doninck, 2023. "Horizontal acquisition of a DNA ligase improves DNA damage tolerance in eukaryotes," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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