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PreprintCited by 10Genomics and Chromatin DynamicsBacterial Genetics and BiotechnologyDNA Repair Mechanisms

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Chromosomal domain formation by archaeal SMC, a roadblock protein, and DNA structure

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Yamaura, Kodai, Takemata, Naomichi, Kariya, Masashi, Ishino, Sonoko, Yamauchi, Masataka, Takada, Shoji, Ishino, Yoshizumi, Atomi, Haruyuki·2024·Nature Communications
DOI 10.1101/2024.05.14.594075PMC PMC11840125

Preprint — published as 10.1038/s41467-025-56197-y

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Abstract

SUMMARY: Structural maintenance of chromosomes (SMC) complexes fold genomes by extruding DNA loops. In eukaryotes, loop-extruding SMC complexes form topologically associating domains (TADs) by being stalled by roadblock proteins. It remains unclear whether a similar mechanism of domain formation exists in prokaryotes. Using high-resolution chromosome conformation capture sequencing, we show that an archaeal homolog of the bacterial Smc-ScpAB complex organizes the genome of Thermococcus kodakarensis into TAD-like domains. We also find that TrmBL2, a nucleoid- associated protein that forms a stiff nucleoprotein filament, stalls the T. kodakarensis SMC complex and establishes a boundary at the site-specific recombination site dif . TrmBL2 stalls the SMC complex at tens of additional non-boundary loci with lower efficiency. Intriguingly, the stalling efficiency is correlated with structural properties of underlying DNA sequences. Our study illuminates not only a eukaryotic-like mechanism of domain formation in archaea, but also an unforeseen role of intrinsic DNA structure in large-scale genome organization.

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Metadata

Authors
Yamaura, K., Takemata, N., Kariya, M., Ishino, S., Yamauchi, M., Takada, S., Ishino, Y., & Atomi, H.
Affiliations
  • Kyoto University (JP)
  • Kyushu University (JP)
Corresponding author
  • Takemata, Naomichi
  • Atomi, Haruyuki
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2024-05-14
Volume
16
Issue
1
Pages
1312-1312
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2024.05.14.594075
PMC
PMC11840125
OpenAlex
W4407751995
Cited by
10
References
1
Citations by year
2026: 3 · 2025: 7
FWCI
2.99
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Nature Communications (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Kyoto University Research Information Repository (Kyoto University) (submittedVersion, cc-by-nc-nd)
Funders
  • Takeda Science Foundation
  • Uehara Memorial Foundation
  • Ministry of Education, Culture, Sports, Science and Technology (JPMJFR224V, JPMJSP2110, JPMJPR20K7, JPMJFS2123, JP23H04281, JP19K22289, JP21K20636, JP20H05934)
  • Japan Society for the Promotion of Science (JP21K20636, JP23H04281, 22K15083, 24K01991, 19K22289, 23K21151, JP20H05934)
  • Japan Science and Technology Agency (JPMJFS2123, JPMJSP2110, JPMJPR20K7, JPMJFR224V)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Keywords
structural maintenance of chromosomes, SMC complex, topologically associating domains, Thermococcus kodakarensis, nucleoid-associated proteins, DNA loop extrusion, site-specific recombination, DNA structure, chromosome conformation
MeSH terms
Nucleic Acid Conformation, DNA, Archaeal, Thermococcus, Archaeal Proteins, Chromosomes, Archaeal, Genome, Archaeal

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