IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28471-w.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28471-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28471-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ruby Yu & Xiaoyi Wang & Danesh Moazed, 2018. "Epigenetic inheritance mediated by coupling of RNAi and histone H3K9 methylation," Nature, Nature, vol. 558(7711), pages 615-619, June.
    2. Gloria Jih & Nahid Iglesias & Mark A. Currie & Natarajan V. Bhanu & Joao A. Paulo & Steven P. Gygi & Benjamin A. Garcia & Danesh Moazed, 2017. "Unique roles for histone H3K9me states in RNAi and heritable silencing of transcription," Nature, Nature, vol. 547(7664), pages 463-467, July.
    3. Jean-François Flot & Boris Hespeels & Xiang Li & Benjamin Noel & Irina Arkhipova & Etienne G. J. Danchin & Andreas Hejnol & Bernard Henrissat & Romain Koszul & Jean-Marc Aury & Valérie Barbe & Roxane-, 2013. "Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga," Nature, Nature, vol. 500(7463), pages 453-457, August.
    4. Andrea Frapporti & Caridad Miró Pina & Olivier Arnaiz & Daniel Holoch & Takayuki Kawaguchi & Adeline Humbert & Evangelia Eleftheriou & Bérangère Lombard & Damarys Loew & Linda Sperling & Karine Guitot, 2019. "The Polycomb protein Ezl1 mediates H3K9 and H3K27 methylation to repress transposable elements in Paramecium," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    5. Ansgar Zoch & Tania Auchynnikava & Rebecca V. Berrens & Yuka Kabayama & Theresa Schöpp & Madeleine Heep & Lina Vasiliauskaitė & Yuvia A. Pérez-Rico & Atlanta G. Cook & Alena Shkumatava & Juri Rappsilb, 2020. "SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation," Nature, Nature, vol. 584(7822), pages 635-639, August.
    6. Dirk Schübeler, 2015. "Function and information content of DNA methylation," Nature, Nature, vol. 517(7534), pages 321-326, January.
    7. Dan Dominissini & Sharon Moshitch-Moshkovitz & Schraga Schwartz & Mali Salmon-Divon & Lior Ungar & Sivan Osenberg & Karen Cesarkas & Jasmine Jacob-Hirsch & Ninette Amariglio & Martin Kupiec & Rotem So, 2012. "Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq," Nature, Nature, vol. 485(7397), pages 201-206, May.
    8. Olga A. Vakhrusheva & Elena A. Mnatsakanova & Yan R. Galimov & Tatiana V. Neretina & Evgeny S. Gerasimov & Sergey A. Naumenko & Svetlana G. Ozerova & Arthur O. Zalevsky & Irina A. Yushenova & Fernando, 2020. "Genomic signatures of recombination in a natural population of the bdelloid rotifer Adineta vaga," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    9. Chuan Ku & Shijulal Nelson-Sathi & Mayo Roettger & Filipa L. Sousa & Peter J. Lockhart & David Bryant & Einat Hazkani-Covo & James O. McInerney & Giddy Landan & William F. Martin, 2015. "Endosymbiotic origin and differential loss of eukaryotic genes," Nature, Nature, vol. 524(7566), pages 427-432, August.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    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. Caojie Liu & Qiuchan Xiong & Qiwen Li & Weimin Lin & Shuang Jiang & Danting Zhang & Yuan Wang & Xiaobo Duan & Ping Gong & Ning Kang, 2022. "CHD7 regulates bone-fat balance by suppressing PPAR-γ signaling," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Zhen-Dong Zhong & Ying-Yuan Xie & Hong-Xuan Chen & Ye-Lin Lan & Xue-Hong Liu & Jing-Yun Ji & Fu Wu & Lingmei Jin & Jiekai Chen & Daniel W. Mak & Zhang Zhang & Guan-Zheng Luo, 2023. "Systematic comparison of tools used for m6A mapping from nanopore direct RNA sequencing," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Zhiyuan Luo & Jiacheng Zhang & Jingyi Fei & Shengdong Ke, 2022. "Deep learning modeling m6A deposition reveals the importance of downstream cis-element sequences," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Lisa-Marie Appel & Vedran Franke & Johannes Benedum & Irina Grishkovskaya & Xué Strobl & Anton Polyansky & Gregor Ammann & Sebastian Platzer & Andrea Neudolt & Anna Wunder & Lena Walch & Stefanie Kais, 2023. "The SPOC domain is a phosphoserine binding module that bridges transcription machinery with co- and post-transcriptional regulators," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    6. Amy L. Hughes & Aleksander T. Szczurek & Jessica R. Kelley & Anna Lastuvkova & Anne H. Turberfield & Emilia Dimitrova & Neil P. Blackledge & Robert J. Klose, 2023. "A CpG island-encoded mechanism protects genes from premature transcription termination," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Simone Mozzachiodi & Lorenzo Tattini & Agnes Llored & Agurtzane Irizar & Neža Škofljanc & Melania D’Angiolo & Matteo De Chiara & Benjamin P. Barré & Jia-Xing Yue & Angela Lutazi & Sophie Loeillet & Ra, 2021. "Aborting meiosis allows recombination in sterile diploid yeast hybrids," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    8. Sakshi Jain & Lukasz Koziej & Panagiotis Poulis & Igor Kaczmarczyk & Monika Gaik & Michal Rawski & Namit Ranjan & Sebastian Glatt & Marina V. Rodnina, 2023. "Modulation of translational decoding by m6A modification of mRNA," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Guoqiang Zhang & Yongru Xu & Xiaona Wang & Yuanxiang Zhu & Liangliang Wang & Wenxin Zhang & Yiru Wang & Yajie Gao & Xuna Wu & Ying Cheng & Qinmiao Sun & Dahua Chen, 2022. "Dynamic FMR1 granule phase switch instructed by m6A modification contributes to maternal RNA decay," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. Pierre Klein & Marija Petrić Howe & Jasmine Harley & Harry Crook & Sofia Esteban Serna & Theodoros I. Roumeliotis & Jyoti S. Choudhary & Anob M. Chakrabarti & Raphaëlle Luisier & Rickie Patani & Andre, 2024. "m6a methylation orchestrates IMP1 regulation of microtubules during human neuronal differentiation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. P Acera Mateos & A J Sethi & A Ravindran & A Srivastava & K Woodward & S Mahmud & M Kanchi & M Guarnacci & J Xu & Z W S Yuen & Y Zhou & A Sneddon & W Hamilton & J Gao & L M Starrs & R Hayashi & V Wick, 2024. "Prediction of m6A and m5C at single-molecule resolution reveals a transcriptome-wide co-occurrence of RNA modifications," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Zhaohui Qin & Ben Li & Karen N. Conneely & Hao Wu & Ming Hu & Deepak Ayyala & Yongseok Park & Victor X. Jin & Fangyuan Zhang & Han Zhang & Li Li & Shili Lin, 2016. "Statistical Challenges in Analyzing Methylation and Long-Range Chromosomal Interaction Data," Statistics in Biosciences, Springer;International Chinese Statistical Association, vol. 8(2), pages 284-309, October.
    13. Liina Nagirnaja & Alexandra M. Lopes & Wu-Lin Charng & Brian Miller & Rytis Stakaitis & Ieva Golubickaite & Alexandra Stendahl & Tianpengcheng Luan & Corinna Friedrich & Eisa Mahyari & Eloise Fadial &, 2022. "Diverse monogenic subforms of human spermatogenic failure," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    14. Xiangyu Wang & Yan Ding & Ran Li & Rujun Zhang & Xuejun Ge & Ruifang Gao & Miao Wang & Yubing Huang & Fang Zhang & Bin Zhao & Wang Liao & Jie Du, 2023. "N6-methyladenosine of Spi2a attenuates inflammation and sepsis-associated myocardial dysfunction in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Kate M. MacDonald & Shirony Nicholson-Puthenveedu & Maha M. Tageldein & Sarika Khasnis & Cheryl H. Arrowsmith & Shane M. Harding, 2023. "Antecedent chromatin organization determines cGAS recruitment to ruptured micronuclei," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Qiang Luo & Jiezhen Mo & Hao Chen & Zetao Hu & Baihui Wang & Jiabing Wu & Ziyu Liang & Wenhao Xie & Kangxi Du & Maolin Peng & Yingping Li & Tianyang Li & Yangyi Zhang & Xiaoyan Shi & Wen-Hui Shen & Ya, 2022. "Structural insights into molecular mechanism for N6-adenosine methylation by MT-A70 family methyltransferase METTL4," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    17. Katja Hartstock & Nadine A. Kueck & Petr Spacek & Anna Ovcharenko & Sabine Hüwel & Nicolas V. Cornelissen & Amarnath Bollu & Christoph Dieterich & Andrea Rentmeister, 2023. "MePMe-seq: antibody-free simultaneous m6A and m5C mapping in mRNA by metabolic propargyl labeling and sequencing," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    18. Belinda Baquero-Pérez & Ivaylo D. Yonchev & Anna Delgado-Tejedor & Rebeca Medina & Mireia Puig-Torrents & Ian Sudbery & Oguzhan Begik & Stuart A. Wilson & Eva Maria Novoa & Juana Díez, 2024. "N6-methyladenosine modification is not a general trait of viral RNA genomes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    19. 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.
    20. You Wu & Wenna Shao & Mengxiao Yan & Yuqin Wang & Pengfei Xu & Guoqiang Huang & Xiaofei Li & Brian D. Gregory & Jun Yang & Hongxia Wang & Xiang Yu, 2024. "Transfer learning enables identification of multiple types of RNA modifications using nanopore direct RNA sequencing," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28471-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.