IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52484-2.html
   My bibliography  Save this article

Creating a bacterium that forms eukaryotic nucleosome core particles

Author

Listed:
  • Xinyun Jing

    (Chinese Academy of Sciences)

  • Niubing Zhang

    (Chinese Academy of Sciences
    East China University of Science and Technology)

  • Xiaojuan Zhou

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Ping Chen

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Jie Gong

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Kaixiang Zhang

    (Chinese Academy of Sciences
    East China University of Science and Technology
    University of Chinese Academy of Sciences)

  • Xueting Wu

    (Chinese Academy of Sciences)

  • Wenjuan Cai

    (Chinese Academy of Sciences)

  • Bang-Ce Ye

    (East China University of Science and Technology)

  • Pei Hao

    (University of Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Guo-ping Zhao

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Sheng Yang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xuan Li

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

The nucleosome is one of the hallmarks of eukaryotes, a dynamic platform that supports many critical functions in eukaryotic cells. Here, we engineer the in vivo assembly of the nucleosome core in the model bacterium Escherichia coli. We show that bacterial chromosome DNA and eukaryotic histones can assemble in vivo to form nucleosome complexes with many features resembling those found in eukaryotes. The formation of nucleosomes in E. coli was visualized with atomic force microscopy and using tripartite split green fluorescent protein. Under a condition that moderate histones expression was induced at 1 µM IPTG, the nucleosome-forming bacterium is viable and has sustained growth for at least 110 divisions in longer-term growth experiments. It exhibits stable nucleosome formation, a consistent transcriptome across passages, and reduced growth fitness under stress conditions. In particular, the nucleosome arrays in E. coli genic regions have profiles resembling those in eukaryotic cells. The observed compatibility between the eukaryotic nucleosome and the bacterial chromosome machinery may reflect a prerequisite for bacteria-archaea union, providing insight into eukaryogenesis and the origin of the nucleosome.

Suggested Citation

  • Xinyun Jing & Niubing Zhang & Xiaojuan Zhou & Ping Chen & Jie Gong & Kaixiang Zhang & Xueting Wu & Wenjuan Cai & Bang-Ce Ye & Pei Hao & Guo-ping Zhao & Sheng Yang & Xuan Li, 2024. "Creating a bacterium that forms eukaryotic nucleosome core particles," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52484-2
    DOI: 10.1038/s41467-024-52484-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52484-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-52484-2?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. Mami Oikawa & Angela Simeone & Eva Hormanseder & Marta Teperek & Vincent Gaggioli & Alan O’Doherty & Emma Falk & Matthieu Sporniak & Clive D’Santos & Valar Nila Roamio Franklin & Kamal Kishore & Charl, 2020. "Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    3. Karolin Luger & Armin W. Mäder & Robin K. Richmond & David F. Sargent & Timothy J. Richmond, 1997. "Crystal structure of the nucleosome core particle at 2.8 Å resolution," Nature, Nature, vol. 389(6648), pages 251-260, September.
    4. Timothy J. Richmond & Curt A. Davey, 2003. "The structure of DNA in the nucleosome core," Nature, Nature, vol. 423(6936), pages 145-150, May.
    5. Noam Kaplan & Irene K. Moore & Yvonne Fondufe-Mittendorf & Andrea J. Gossett & Desiree Tillo & Yair Field & Emily M. LeProust & Timothy R. Hughes & Jason D. Lieb & Jonathan Widom & Eran Segal, 2009. "The DNA-encoded nucleosome organization of a eukaryotic genome," Nature, Nature, vol. 458(7236), pages 362-366, March.
    Full references (including those not matched with items on IDEAS)

    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. Marko Dunjić & Felix Jonas & Gilad Yaakov & Roye More & Yoav Mayshar & Yoach Rais & Ayelet-Hashahar Orenbuch & Saifeng Cheng & Naama Barkai & Yonatan Stelzer, 2023. "Histone exchange sensors reveal variant specific dynamics in mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Namrata Kumar & Arjan F. Theil & Vera Roginskaya & Yasmin Ali & Michael Calderon & Simon C. Watkins & Ryan P. Barnes & Patricia L. Opresko & Alex Pines & Hannes Lans & Wim Vermeulen & Bennett Houten, 2022. "Global and transcription-coupled repair of 8-oxoG is initiated by nucleotide excision repair proteins," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Poonam Dhillon & Kelly Ann Mulholland & Hailong Hu & Jihwan Park & Xin Sheng & Amin Abedini & Hongbo Liu & Allison Vassalotti & Junnan Wu & Katalin Susztak, 2023. "Increased levels of endogenous retroviruses trigger fibroinflammation and play a role in kidney disease development," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Gaylor Boulay & Liliane C. Broye & Rui Dong & Sowmya Iyer & Rajendran Sanalkumar & Yu-Hang Xing & Rémi Buisson & Shruthi Rengarajan & Beverly Naigles & Benoît Duc & Angela Volorio & Mary E. Awad & Raf, 2024. "EWS-WT1 fusion isoforms establish oncogenic programs and therapeutic vulnerabilities in desmoplastic small round cell tumors," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Teresa Maria Rosaria Noviello & Anna Maria Giacomo & Francesca Pia Caruso & Alessia Covre & Roberta Mortarini & Giovanni Scala & Maria Claudia Costa & Sandra Coral & Wolf H. Fridman & Catherine Sautès, 2023. "Guadecitabine plus ipilimumab in unresectable melanoma: five-year follow-up and integrated multi-omic analysis in the phase 1b NIBIT-M4 trial," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Kate E. Stanley & Tatjana Jatsenko & Stefania Tuveri & Dhanya Sudhakaran & Lore Lannoo & Kristel Calsteren & Marie Borre & Ilse Parijs & Leen Coillie & Kris Bogaert & Rodrigo Almeida Toledo & Liesbeth, 2024. "Cell type signatures in cell-free DNA fragmentation profiles reveal disease biology," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Segal Mark R, 2008. "Re-Cracking the Nucleosome Positioning Code," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 7(1), pages 1-24, April.
    9. Michaël Noë & Dimitrios Mathios & Akshaya V. Annapragada & Shashikant Koul & Zacharia H. Foda & Jamie E. Medina & Stephen Cristiano & Christopher Cherry & Daniel C. Bruhm & Noushin Niknafs & Vilmos Ad, 2024. "DNA methylation and gene expression as determinants of genome-wide cell-free DNA fragmentation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    10. Wilfried Engl & Aliz Kunstar-Thomas & Siyi Chen & Woei Shyuan Ng & Hendrik Sielaff & Ziqing Winston Zhao, 2024. "Single-molecule imaging of SWI/SNF chromatin remodelers reveals bromodomain-mediated and cancer-mutants-specific landscape of multi-modal DNA-binding dynamics," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    11. Xiaohe Lin & Junjie Yin & Yifan Wang & Jing Yao & Qingshun Q. Li & Vit Latzel & Oliver Bossdorf & Yuan-Ye Zhang, 2024. "Environment-induced heritable variations are common in Arabidopsis thaliana," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    12. Quentin I. B. Lemaître & Natascha Bartsch & Ian U. Kouzel & Henriette Busengdal & Gemma Sian Richards & Patrick R. H. Steinmetz & Fabian Rentzsch, 2023. "NvPrdm14d-expressing neural progenitor cells contribute to non-ectodermal neurogenesis in Nematostella vectensis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Songming Tang & Xuejian Cui & Rongxiang Wang & Sijie Li & Siyu Li & Xin Huang & Shengquan Chen, 2024. "scCASE: accurate and interpretable enhancement for single-cell chromatin accessibility sequencing data," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Raúl F. Pérez & Patricia Tezanos & Alfonso Peñarroya & Alejandro González-Ramón & Rocío G. Urdinguio & Javier Gancedo-Verdejo & Juan Ramón Tejedor & Pablo Santamarina-Ojeda & Juan José Alba-Linares & , 2024. "A multiomic atlas of the aging hippocampus reveals molecular changes in response to environmental enrichment," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    15. Yanming Ren & Zongyao Huang & Lingling Zhou & Peng Xiao & Junwei Song & Ping He & Chuanxing Xie & Ran Zhou & Menghan Li & Xiangqun Dong & Qing Mao & Chao You & Jianguo Xu & Yanhui Liu & Zhigang Lan & , 2023. "Spatial transcriptomics reveals niche-specific enrichment and vulnerabilities of radial glial stem-like cells in malignant gliomas," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    16. Tiago C. Luis & Nikolaos Barkas & Joana Carrelha & Alice Giustacchini & Stefania Mazzi & Ruggiero Norfo & Bishan Wu & Affaf Aliouat & Jose A. Guerrero & Alba Rodriguez-Meira & Tiphaine Bouriez-Jones &, 2023. "Perivascular niche cells sense thrombocytopenia and activate hematopoietic stem cells in an IL-1 dependent manner," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    17. Masaki Kikuchi & Satoshi Morita & Masatoshi Wakamori & Shin Sato & Tomomi Uchikubo-Kamo & Takehiro Suzuki & Naoshi Dohmae & Mikako Shirouzu & Takashi Umehara, 2023. "Epigenetic mechanisms to propagate histone acetylation by p300/CBP," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    18. Fritz Nagae & Yasuto Murayama & Tsuyoshi Terakawa, 2024. "Molecular mechanism of parental H3/H4 recycling at a replication fork," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. Michael R. Kelly & Kamila Wisniewska & Matthew J. Regner & Michael W. Lewis & Andrea A. Perreault & Eric S. Davis & Douglas H. Phanstiel & Joel S. Parker & Hector L. Franco, 2022. "A multi-omic dissection of super-enhancer driven oncogenic gene expression programs in ovarian cancer," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    20. Wolfram Möbius & Ulrich Gerland, 2010. "Quantitative Test of the Barrier Nucleosome Model for Statistical Positioning of Nucleosomes Up- and Downstream of Transcription Start Sites," PLOS Computational Biology, Public Library of Science, vol. 6(8), pages 1-11, August.

    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:15:y:2024:i:1:d:10.1038_s41467-024-52484-2. 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.