Crystal structure and initial characterization of a novel archaeal-like Holliday junction-resolving enzyme from Thermus thermophilus phage Tth15-6.

archaeal-like Holliday junction-resolving enzymes signature motifs structure–function relationship thermophilic bacteriophages

Journal

Acta crystallographica. Section D, Structural biology
ISSN: 2059-7983
Titre abrégé: Acta Crystallogr D Struct Biol
Pays: United States
ID NLM: 101676043

Informations de publication

Date de publication:
01 Feb 2022
Historique:
received: 04 08 2021
accepted: 19 11 2021
entrez: 1 2 2022
pubmed: 2 2 2022
medline: 5 4 2022
Statut: ppublish

Résumé

This study describes the production, characterization and structure determination of a novel Holliday junction-resolving enzyme. The enzyme, termed Hjc_15-6, is encoded in the genome of phage Tth15-6, which infects Thermus thermophilus. Hjc_15-6 was heterologously produced in Escherichia coli and high yields of soluble and biologically active recombinant enzyme were obtained in both complex and defined media. Amino-acid sequence and structure comparison suggested that the enzyme belongs to a group of enzymes classified as archaeal Holliday junction-resolving enzymes, which are typically divalent metal ion-binding dimers that are able to cleave X-shaped dsDNA-Holliday junctions (Hjs). The crystal structure of Hjc_15-6 was determined to 2.5 Å resolution using the selenomethionine single-wavelength anomalous dispersion method. To our knowledge, this is the first crystal structure of an Hj-resolving enzyme originating from a bacteriophage that can be classified as an archaeal type of Hj-resolving enzyme. As such, it represents a new fold for Hj-resolving enzymes from phages. Characterization of the structure of Hjc_15-6 suggests that it may form a dimer, or even a homodimer of dimers, and activity studies show endonuclease activity towards Hjs. Furthermore, based on sequence analysis it is proposed that Hjc_15-6 has a three-part catalytic motif corresponding to E-SD-EVK, and this motif may be common among other Hj-resolving enzymes originating from thermophilic bacteriophages.

Identifiants

pubmed: 35102887
pii: S2059798321012298
doi: 10.1107/S2059798321012298
pmc: PMC8805305
doi:

Substances chimiques

DNA, Cruciform 0
Holliday Junction Resolvases EC 3.1.21.-

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

212-227

Subventions

Organisme : Horizon 2020 Framework Programme, European Metrology Programme for Innovation and Research
ID : 685778

Informations de copyright

open access.

Références

J Biol Chem. 2016 May 20;291(21):11094-104
pubmed: 27013661
Cold Spring Harb Perspect Biol. 2014 Sep 02;6(9):a023192
pubmed: 25183833
BMC Genomics. 2008 Feb 08;9:75
pubmed: 18261238
Science. 1998 Apr 10;280(5361):279-84
pubmed: 9535656
BMC Bioinformatics. 2005 Jul 12;6:172
pubmed: 16011798
Nat Struct Biol. 2001 Jan;8(1):62-7
pubmed: 11135673
Sci Rep. 2020 Jan 15;10(1):393
pubmed: 31941902
EMBO J. 2004 Aug 4;23(15):2972-81
pubmed: 15257292
J Mol Biol. 2008 Apr 25;378(2):468-80
pubmed: 18355836
Protein Sci. 2020 Jan;29(1):128-140
pubmed: 31606894
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549
pubmed: 29722887
J Basic Microbiol. 2010 Oct;50(5):452-6
pubmed: 20806260
Nature. 2007 Oct 4;449(7162):616-20
pubmed: 17873859
Nucleic Acids Res. 2012 Aug;40(15):7016-45
pubmed: 22638584
J Mol Biol. 2000 Apr 7;297(4):923-32
pubmed: 10736227
Nucleic Acids Res. 2020 Jan 8;48(D1):D265-D268
pubmed: 31777944
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):355-67
pubmed: 21460454
Biochem Biophys Res Commun. 2008 Dec 5;377(1):89-92
pubmed: 18831965
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Mol Microbiol. 2013 Sep;89(6):1240-58
pubmed: 23888987
Cell. 1994 Sep 23;78(6):1063-72
pubmed: 7923356
IUCrJ. 2018 Jan 25;5(Pt 2):166-171
pubmed: 29765606
Structure. 2001 Mar 7;9(3):197-204
pubmed: 11286886
Nucleic Acids Res. 2021 Jan 8;49(D1):D344-D354
pubmed: 33156333
Nucleic Acids Res. 2016 Jan 4;44(D1):D7-19
pubmed: 26615191
Microb Ecol. 2001 Aug;42(2):117-125
pubmed: 12024275
J Virol. 1976 Jun;18(3):1000-15
pubmed: 775128
Appl Environ Microbiol. 2009 Jan;75(1):212-23
pubmed: 18997032
Biotechnol Lett. 2005 Jul;27(14):983-90
pubmed: 16132841
Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):8873-8
pubmed: 10430863
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):386-94
pubmed: 21460457
J Mol Biol. 2006 Dec 8;364(4):667-77
pubmed: 17027029
J Mol Biol. 2007 Sep 21;372(3):774-97
pubmed: 17681537
FEMS Microbiol Lett. 2021 Jun 24;368(12):
pubmed: 34114607
Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9351-3
pubmed: 10944205
Nucleic Acids Res. 2000 Nov 15;28(22):4544-51
pubmed: 11071944
J Virol. 1976 Jun;18(3):992-9
pubmed: 775132
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Cell. 1982 Jun;29(2):357-65
pubmed: 6288255
Acta Crystallogr Sect F Struct Biol Cryst Commun. 2007 Sep 1;63(Pt 9):802-6
pubmed: 17768360
Nucleic Acids Res. 2000 Sep 15;28(18):3417-32
pubmed: 10982859
J Virol. 2009 Sep;83(18):9388-97
pubmed: 19587059
Nucleic Acids Res. 2000 Nov 15;28(22):4540-3
pubmed: 11071943
J Biol Chem. 2009 Jan 9;284(2):1190-201
pubmed: 19004818
Bioinformatics. 2009 May 1;25(9):1189-91
pubmed: 19151095
Bacteriophage. 2011 May;1(3):152-164
pubmed: 22164349
Mol Cell Proteomics. 2013 Jan;12(1):14-28
pubmed: 23001859
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32
pubmed: 20124692
Nucleic Acids Res. 2011 Mar;39(4):1187-96
pubmed: 20961958
FEBS Lett. 2017 Apr;591(8):1073-1082
pubmed: 27990631
J Mol Biol. 2001 Jun 22;309(5):1067-76
pubmed: 11399079
Nucleic Acids Res. 2005 Jun 22;33(11):3598-605
pubmed: 15972856
EMBO J. 1999 Mar 15;18(6):1447-58
pubmed: 10075917
Biochemistry. 2001 Jan 16;40(2):387-94
pubmed: 11148032
Nucleic Acids Res. 2014 Jul;42(12):7489-527
pubmed: 24878924
Proteins. 1994 Nov;20(3):279-82
pubmed: 7892176
Nucleic Acids Res. 2001 Sep 15;29(18):3705-27
pubmed: 11557805
Nucleic Acids Res. 2017 Apr 7;45(6):3580-3590
pubmed: 28100693
Arch Virol. 2006 Apr;151(4):663-79
pubmed: 16308675
Proc Natl Acad Sci U S A. 2001 May 8;98(10):5509-14
pubmed: 11331763
Cell Mol Life Sci. 2005 Mar;62(6):685-707
pubmed: 15770420
Biol Direct. 2016 Oct 21;11(1):55
pubmed: 27769290

Auteurs

Josefin Ahlqvist (J)

Biotechnology, Department of Chemistry, Lund University, PO Box 124, 221 00 Lund, Sweden.

Javier A Linares-Pastén (JA)

Biotechnology, Department of Chemistry, Lund University, PO Box 124, 221 00 Lund, Sweden.

Maria Håkansson (M)

SARomics Biostructures, Medicon Village, 223 81 Lund, Sweden.

Andrius Jasilionis (A)

Biotechnology, Department of Chemistry, Lund University, PO Box 124, 221 00 Lund, Sweden.

Karolina Kwiatkowska-Semrau (K)

Laboratory of Extremophiles Biology, Department of Microbiology, Faculty of Biology, University of Gdansk, ul. Wita Stwosza 59, 80-308 Gdansk, Poland.

Ólafur H Friðjónsson (ÓH)

Matís, Vínlandsleið 12, 113 Reykjavík, Iceland.

Anna Karina Kaczorowska (AK)

Collection of Plasmids and Microorganisms, University of Gdansk, ul. Wita Stwosza 59, Gdansk 80-308, Poland.

Slawomir Dabrowski (S)

A&A Biotechnology, al. Zwycięstwa 96/98, 81-451 Gdynia, Poland.

Arnþór Ævarsson (A)

Matís, Vínlandsleið 12, 113 Reykjavík, Iceland.

Guðmundur Ó Hreggviðsson (GÓ)

Matís, Vínlandsleið 12, 113 Reykjavík, Iceland.

Salam Al-Karadaghi (S)

SARomics Biostructures, Medicon Village, 223 81 Lund, Sweden.

Tadeusz Kaczorowski (T)

Laboratory of Extremophiles Biology, Department of Microbiology, Faculty of Biology, University of Gdansk, ul. Wita Stwosza 59, 80-308 Gdansk, Poland.

Eva Nordberg Karlsson (E)

Biotechnology, Department of Chemistry, Lund University, PO Box 124, 221 00 Lund, Sweden.

Articles similaires

Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Lakes Salinity Archaea Bacteria Microbiota
Host Specificity Bacteriophages Genomics Algorithms Escherichia coli
Animals Enterococcus faecalis Levodopa Bacteriophages Gastrointestinal Microbiome

Classifications MeSH