In vivo assembly of complete eukaryotic nucleosomes and (H3-H4)-only non-canonical nucleosomal particles in the model bacterium Escherichia coli

Xiaojuan Zhou; Niubing Zhang; Jie Gong; Kaixiang Zhang; Ping Chen; Xiang Cheng; Bang-Ce Ye; Guoping Zhao; Xinyun Jing; Xuan Li

doi:10.1038/s42003-024-07211-4

In vivo assembly of complete eukaryotic nucleosomes and (H3-H4)-only non-canonical nucleosomal particles in the model bacterium Escherichia coli

Commun Biol. 2024 Nov 14;7(1):1510. doi: 10.1038/s42003-024-07211-4.

Authors

Xiaojuan Zhou^#^{1

2}, Niubing Zhang^#^{1

2

3}, Jie Gong^{1

2}, Kaixiang Zhang^{1

2

3}, Ping Chen¹, Xiang Cheng^{1

2}, Bang-Ce Ye³, Guoping Zhao^{4

5

6}, Xinyun Jing⁷, Xuan Li^{8

9}

Affiliations

¹ Key Laboratory of Synthetic Biology, Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China.
² University of Chinese Academy of Sciences, 100039, Beijing, China.
³ State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai, 200237, China.
⁴ Key Laboratory of Synthetic Biology, Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China. [email protected].
⁵ Key Laboratory of Systems Health Science of Zhejiang Province, School of Life Science, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou, China. [email protected].
⁶ Department of Microbiology and Microbial Engineering, School of Life Sciences, Fudan University, Shanghai, China. [email protected].
⁷ Key Laboratory of Synthetic Biology, Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China. [email protected].
⁸ Key Laboratory of Synthetic Biology, Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200032, China. [email protected].
⁹ University of Chinese Academy of Sciences, 100039, Beijing, China. [email protected].

^# Contributed equally.

PMID: 39543208
DOI: 10.1038/s42003-024-07211-4

Abstract

As a fundamental unit for packaging genomic DNA into chromatin, the eukaryotic nucleosome core comprises a canonical octamer with two copies for each histone, H2A, H2B, H3, and H4, wrapped around with 147 base pairs of DNA. While H3 and H4 share structure-fold with archaeal histone-like proteins, the eukaryotic nucleosome core and the complete nucleosome (the core plus H1 histone) are unique to eukaryotes. To explore whether the eukaryotic nucleosome can assemble in prokaryotes and to reconstruct the possible route for its emergence in eukaryogenesis, we developed an in vivo system for assembly of nucleosomes in the model bacterium, Escherichia coli, and successfully reconstituted the core nucleosome, the complete nucleosome, and unexpectedly the non-canonical (H3-H4)₄ octasome. The core and complete nucleosomes assembled in E. coli exhibited footprints typical of eukaryotic hosts after in situ micrococcal nuclease digestion. Additionally, they caused condensation of E. coli nucleoid. We also demonstrated the stable formation of non-canonical (H3-H4)₂ tetrasome and (H3-H4)₄ octasomes in vivo, which are suggested to be 'fossil complex' that marks the intermediate in the progressive development of eukaryotic nucleosome. The study presents a unique platform in a bacterium for in vivo assembly and studying the properties of non-canonical variants of nucleosome.