Crystal structure of the Redβ C-terminal domain in complex with λ Exonuclease reveals an unexpected homology with λ Orf and an interaction with Escherichia coli single stranded DNA binding protein

Caldwell, Brian J.; Zakharova, Ekaterina; Filsinger, Gabriel T.; Wannier, Timothy M.; Hempfling, Jordan P.; Chun-Der, Lee; Pei, Dehua; Church, George M.; Bell, Charles E.

doi:10.1093/nar/gky1309

Title: Crystal structure of the Redβ C-terminal domain in complex with λ Exonuclease reveals an unexpected homology with λ Orf and an interaction with Escherichia coli single stranded DNA binding protein

Journal Article · 08 January 2019 · Nucleic Acids Research

DOI: https://doi.org/10.1093/nar/gky1309 · OSTI ID:1528913

Caldwell, Brian J. ^[1]; Zakharova, Ekaterina ^[2]; Filsinger, Gabriel T. ^[3]; Wannier, Timothy M. ^[3]; Hempfling, Jordan P. ^[2]; Chun-Der, Lee ^[2]; Pei, Dehua ^[2]; Church, George M. ^[4]; Bell, Charles E. ^[2]

The Ohio State Univ., Columbus, OH (United States); Harvard Medical School
The Ohio State Univ., Columbus, OH (United States)
Harvard Medical School, Cambridge, MA (United States)
Harvard Medical School, Cambridge, MA (United States); Harvard Univ., Cambridge, MA (United States)

Bacteriophage λ encodes a DNA recombination system that includes a 5'-3' exonuclease (λ Exo) and a single strand annealing protein (Redβ). The two proteins form a complex that is thought to mediate loading of Redβ directly onto the single-stranded 3'-overhang generated by λ Exo. Here, we present a 2.3 Å crystal structure of the λ Exo trimer bound to three copies of the Redβ C-terminal domain (CTD). Mutation of residues at the hydrophobic core of the interface disrupts complex formation in vitro and impairs recombination in vivo. The Redβ CTD forms a three-helix bundle with unexpected structural homology to phage λ Orf, a protein that binds to E. coli single-stranded DNA binding protein (SSB) to function as a recombination mediator. Based on this relationship, we found that Redβ binds to full-length SSB, and to a peptide corresponding to its nine C-terminal residues, in an interaction that requires the CTD. These results suggest a dual role of the CTD, first in binding to λ Exo to facilitate loading of Redβ directly onto the initial single-stranded DNA (ssDNA) at a 3'-overhang, and second in binding to SSB to facilitate annealing of the overhang to SSB-coated ssDNA at the replication fork.

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Research Organization:: Harvard Medical School, Cambridge, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23). Biological Systems Science Division

Grant/Contract Number:: FG02-02ER63445

OSTI ID:: 1528913

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 4 Vol. 47; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Recombinational Repair of DNA Damage inEscherichia coli and Bacteriophage λ Kuzminov, Andrei Microbiology and Molecular Biology Reviews, Vol. 63, Issue 4 https://doi.org/10.1128/MMBR.63.4.751-813.1999	journal	December 1999
The phage lambda orf gene encodes a trans-acting factor that suppresses Escherichia coli recO, recR, and recF mutations for recombination of lambda but not of E. coli. Sawitzke, J. A.; Stahl, F. W. Journal of Bacteriology, Vol. 176, Issue 21 https://doi.org/10.1128/jb.176.21.6730-6737.1994	journal	November 1994
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Temperate Phages Acquire DNA from Defective Prophages by Relaxed Homologous Recombination: The Role of Rad52-Like Recombinases De Paepe, Marianne; Hutinet, Geoffrey; Son, Olivier PLoS Genetics, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pgen.1004181	journal	March 2014
Improving Lambda Red Genome Engineering in Escherichia coli via Rational Removal of Endogenous Nucleases Mosberg, Joshua A.; Gregg, Christopher J.; Lajoie, Marc J. PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0044638	journal	September 2012
Structural and Functional Characterization of the Redβ Recombinase from Bacteriophage λ Matsubara, Kazuko; Malay, Ali D.; Curtis, Fiona A. PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0078869	journal	November 2013
Phage Orf Family Recombinases: Conservation of Activities and Involvement of the Central Channel in DNA Binding Curtis, Fiona A.; Malay, Ali D.; Trotter, Alexander J. PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0102454	journal	August 2014
An Improved Recombineering Approach by Adding RecA to λ Red Recombination Wang, Junping; Sarov, Mihail; Rientjes, Jeanette Molecular Biotechnology, Vol. 32, Issue 1 https://doi.org/10.1385/MB:32:1:043	journal	January 2006
Dna2 nuclease-helicase structure, mechanism and regulation by Rpa Zhou, Chun; Pourmal, Sergei; Pavletich, Nikola P. eLife, Vol. 4 https://doi.org/10.7554/eLife.09832	journal	November 2015
Structural basis for the inhibition of RecBCD by Gam and its synergistic antibacterial effect with quinolones Wilkinson, Martin; Troman, Lucy; Wan Nur Ismah, Wan AK eLife, Vol. 5 https://doi.org/10.7554/eLife.22963	journal	December 2016

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59 BASIC BIOLOGICAL SCIENCES
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Red-beta
crystal structure

Title: Crystal structure of the Redβ C-terminal domain in complex with λ Exonuclease reveals an unexpected homology with λ Orf and an interaction with Escherichia coli single stranded DNA binding protein

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