DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteins

Abstract Single-stranded DNA-binding proteins (SSBs) protect transiently exposed ssDNA, yet how DNA polymerase (DNAp) displaces them during replication remains unclear. Using single-molecule force spectroscopy, dual-color imaging, and molecular dynamics simulations on bacteriophage T7 DNAp and SSB,...

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Main Authors: Longfu Xu, Shikai Jin, Mia Urem, Seung-Joo Lee, Meindert H. Lamers, Xun Chen, Peter G. Wolynes, Gijs J. L. Wuite
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-62531-1
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author Longfu Xu
Shikai Jin
Mia Urem
Seung-Joo Lee
Meindert H. Lamers
Xun Chen
Peter G. Wolynes
Gijs J. L. Wuite
author_facet Longfu Xu
Shikai Jin
Mia Urem
Seung-Joo Lee
Meindert H. Lamers
Xun Chen
Peter G. Wolynes
Gijs J. L. Wuite
author_sort Longfu Xu
collection DOAJ
description Abstract Single-stranded DNA-binding proteins (SSBs) protect transiently exposed ssDNA, yet how DNA polymerase (DNAp) displaces them during replication remains unclear. Using single-molecule force spectroscopy, dual-color imaging, and molecular dynamics simulations on bacteriophage T7 DNAp and SSB, we investigated molecular mechanisms underlying SSB displacement. T7 SSB modulates replication in a force-dependent manner: enhancing it at low tension by preventing secondary structures while impeding it at high tension. Dual-color imaging shows SSBs remain stationary as DNAp advances, supporting a sequential displacement model. Molecular dynamics suggests that DNAp actively lowers the SSB dissociation energy barrier through interactions mediated by the SSB C-terminal tail. FRET confirms close protein proximity during encounters. Optimal replication requires SSB saturation of ssDNA, establishing a delicate balance between protection and efficiency. This spatiotemporal coordination between DNAp and SSB is critical for resolving molecular collisions and may represent a general mechanism for resolving molecular collisions, ensuring both processivity and genomic integrity.
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publisher Nature Portfolio
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series Nature Communications
spelling doaj-art-17bce899d7154fa8b9d98b7a0f1cd8402025-08-20T03:43:22ZengNature PortfolioNature Communications2041-17232025-08-0116111610.1038/s41467-025-62531-1DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteinsLongfu Xu0Shikai Jin1Mia Urem2Seung-Joo Lee3Meindert H. Lamers4Xun Chen5Peter G. Wolynes6Gijs J. L. Wuite7Department of Physics and Astronomy, and LaserLaB Amsterdam, Vrije Universiteit Amsterdam, De Boelelaan 1081Center for Theoretical Biological Physics, Rice UniversityLeiden University Center of Infectious Diseases (LUCID), Leiden University Medical CenterDepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical SchoolDepartment of Cell and Chemical Biology, Leiden University Medical Center (LUMC)Department of Medicinal Chemistry, National Vaccine Innovation Platform, Nanjing Medical UniversityCenter for Theoretical Biological Physics, Rice UniversityDepartment of Physics and Astronomy, and LaserLaB Amsterdam, Vrije Universiteit Amsterdam, De Boelelaan 1081Abstract Single-stranded DNA-binding proteins (SSBs) protect transiently exposed ssDNA, yet how DNA polymerase (DNAp) displaces them during replication remains unclear. Using single-molecule force spectroscopy, dual-color imaging, and molecular dynamics simulations on bacteriophage T7 DNAp and SSB, we investigated molecular mechanisms underlying SSB displacement. T7 SSB modulates replication in a force-dependent manner: enhancing it at low tension by preventing secondary structures while impeding it at high tension. Dual-color imaging shows SSBs remain stationary as DNAp advances, supporting a sequential displacement model. Molecular dynamics suggests that DNAp actively lowers the SSB dissociation energy barrier through interactions mediated by the SSB C-terminal tail. FRET confirms close protein proximity during encounters. Optimal replication requires SSB saturation of ssDNA, establishing a delicate balance between protection and efficiency. This spatiotemporal coordination between DNAp and SSB is critical for resolving molecular collisions and may represent a general mechanism for resolving molecular collisions, ensuring both processivity and genomic integrity.https://doi.org/10.1038/s41467-025-62531-1
spellingShingle Longfu Xu
Shikai Jin
Mia Urem
Seung-Joo Lee
Meindert H. Lamers
Xun Chen
Peter G. Wolynes
Gijs J. L. Wuite
DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteins
Nature Communications
title DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteins
title_full DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteins
title_fullStr DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteins
title_full_unstemmed DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteins
title_short DNA polymerase actively and sequentially displaces single-stranded DNA-binding proteins
title_sort dna polymerase actively and sequentially displaces single stranded dna binding proteins
url https://doi.org/10.1038/s41467-025-62531-1
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