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Cited by 3Diffusion and Search DynamicsDNA and Nucleic Acid ChemistryBacterial Genetics and Biotechnology

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Short-range translocation by a restriction enzyme motor triggers diffusion along DNA

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Göse, Martin, Magill, Emma E., Hughes-Games, Alex, Shaw, Steven J., Diffin, Fiona M., Rawson, Tara, Nagy, Zsofia, Seidel, Ralf, Szczelkun, Mark D.·2024·Nature Chemical Biology
DOI 10.1038/s41589-023-01504-1PMC PMC11142916

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Abstract

Cleavage of bacteriophage DNA by the Type III restriction-modification enzymes requires long-range interaction between DNA sites. This is facilitated by one-dimensional diffusion (‘DNA sliding’) initiated by ATP hydrolysis catalyzed by a superfamily 2 helicase-like ATPase. Here we combined ultrafast twist measurements based on plasmonic DNA origami nano-rotors with stopped-flow fluorescence and gel-based assays to examine the role(s) of ATP hydrolysis. Our data show that the helicase-like domain has multiple roles. First, this domain stabilizes initial DNA interactions alongside the methyltransferase subunits. Second, it causes environmental changes in the flipped adenine base following hydrolysis of the first ATP. Finally, it remodels nucleoprotein interactions via constrained translocation of a ∼ 5 to 22-bp double stranded DNA loop. Initiation of DNA sliding requires 8–15 bp of DNA downstream of the motor, corresponding to the site of nuclease domain binding. Our data unify previous contradictory communication models for Type III enzymes.

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Metadata

Authors
Göse, M., Magill, E. E., Hughes-Games, A., Shaw, S. J., Diffin, F. M., Rawson, T., Nagy, Z., Seidel, R., & Szczelkun, M. D.
Affiliations
  • Leipzig University (DE)
  • University of Bristol (GB)
Corresponding author
  • Seidel, Ralf
  • Szczelkun, Mark D.
ORCID
Venue
Nature Chemical Biology
Publisher
Springer Science and Business Media LLC
Published
2024-01-02
Volume
20
Issue
6
Pages
689-698
ISSN
  • 1552-4450 (ISSN-L)
  • 1552-4469
DOI
10.1038/s41589-023-01504-1
PMC
PMC11142916
OpenAlex
W4390507632
Cited by
3
References
2
Citations by year
2026: 1 · 2025: 1 · 2024: 1
FWCI
0.41
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Chemical Biology (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Explore Bristol Research (acceptedVersion, cc-by)
  • Bristol Research (University of Bristol) (acceptedVersion, cc-by)
Funders
  • Research Councils UK (EP/L016494/1)
  • European Commission (ERC-2017, 724863, HORIZON2020)
  • Cardiff University
  • University of Bristol (ERC-2017-ADG-788405)
  • Freistaat Sachsen (100382164, SAB 100382164)
  • Engineering and Physical Sciences Research Council (EP/L016494/1)
  • Biotechnology and Biological Sciences Research Council (EP /L016494/1, BB/W019337/1)
  • European Social Fund (SAB 100382164, 100382164)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Diffusion and Search Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
DNA sliding, ATP hydrolysis, DNA translocation, methyltransferase, nuclease domain, phage DNA
MeSH terms
Adenosine Triphosphate, Diffusion, DNA, DNA, Viral, Hydrolysis, Deoxyribonucleases, Type III Site-Specific

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