Z-form extracellular DNA is a structural component of the bacterial biofilm matrix.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
11 11 2021
Historique:
received: 22 01 2021
revised: 03 08 2021
accepted: 12 10 2021
pubmed: 5 11 2021
medline: 7 1 2022
entrez: 4 11 2021
Statut: ppublish

Résumé

Biofilms are community architectures adopted by bacteria inclusive of a self-formed extracellular matrix that protects resident bacteria from diverse environmental stresses and, in many species, incorporates extracellular DNA (eDNA) and DNABII proteins for structural integrity throughout biofilm development. Here, we present evidence that this eDNA-based architecture relies on the rare Z-form. Z-form DNA accumulates as biofilms mature and, through stabilization by the DNABII proteins, confers structural integrity to the biofilm matrix. Indeed, substances known to drive B-DNA into Z-DNA promoted biofilm formation whereas those that drive Z-DNA into B-DNA disrupted extant biofilms. Importantly, we demonstrated that the universal bacterial DNABII family of proteins stabilizes both bacterial- and host-eDNA in the Z-form in situ. A model is proposed that incorporates the role of Z-DNA in biofilm pathogenesis, innate immune response, and immune evasion.

Identifiants

pubmed: 34735796
pii: S0092-8674(21)01220-4
doi: 10.1016/j.cell.2021.10.010
pmc: PMC8595767
mid: NIHMS1748889
pii:
doi:

Substances chimiques

Bacterial Proteins 0
DNA, Bacterial 0
DNA, Cruciform 0
Deoxyribonucleases EC 3.1.-
Tetradecanoylphorbol Acetate NI40JAQ945

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5740-5758.e17

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI155501
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC011818
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM124436
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests S.D.G. and L.O.B. are founders, shareholders, and members of the scientific advisory board of Clarametyx Biosciences, Inc.

Références

J Bacteriol. 2018 May 9;200(11):
pubmed: 29437850
Proc Natl Acad Sci U S A. 1982 Aug;79(15):4560-4
pubmed: 6956879
Nucleic Acids Res. 1983 Mar 25;11(6):1931-41
pubmed: 6835844
J Biol Chem. 1986 May 15;261(14):6438-43
pubmed: 3700399
J Antimicrob Chemother. 2015;70(6):1608-21
pubmed: 25693996
J Rheumatol. 1984 Oct;11(5):633-7
pubmed: 6334742
Nat Struct Mol Biol. 2011 Feb;18(2):169-76
pubmed: 21217697
Environ Microbiol. 2014 Apr;16(4):1040-52
pubmed: 24119133
Biophys J. 1994 Dec;67(6):2454-9
pubmed: 7696484
Appl Environ Microbiol. 2005 Sep;71(9):5404-10
pubmed: 16151131
Science. 1991 Nov 15;254(5034):1003-6
pubmed: 1948069
Cell Cycle. 2010 Oct 15;9(20):4236-44
pubmed: 20948314
J Bacteriol. 2007 May;189(10):3868-75
pubmed: 17322318
Proc Natl Acad Sci U S A. 2019 Dec 10;116(50):25068-25077
pubmed: 31767757
Mol Microbiol. 2014 Sep;93(6):1246-58
pubmed: 25069521
Acta Paediatr. 2006 Sep;95(9):1070-4
pubmed: 16938752
Sci Rep. 2018 Jan 17;8(1):914
pubmed: 29343810
Proc Natl Acad Sci U S A. 1982 Mar;79(6):1771-5
pubmed: 6952228
J Biol Chem. 1982 Oct 25;257(20):12081-5
pubmed: 7118931
Infect Immun. 2000 Apr;68(4):2119-28
pubmed: 10722609
PLoS One. 2013 Jun 14;8(6):e67629
pubmed: 23799151
J Virol. 2002 Jun;76(11):5654-66
pubmed: 11991994
PLoS One. 2012;7(4):e35558
pubmed: 22530050
Mol Immunol. 1992 May;29(5):609-17
pubmed: 1584229
J Mol Biol. 2007 Jan 26;365(4):1005-16
pubmed: 17097674
Nat Commun. 2019 Apr 10;10(1):1667
pubmed: 30971685
Front Microbiol. 2017 Jul 26;8:1390
pubmed: 28798731
Vaccine. 2013 Jul 25;31(34):3417-26
pubmed: 23092856
Synth Syst Biotechnol. 2020 Jan 13;5(1):1-10
pubmed: 31956705
Biophys J. 2000 Feb;78(2):1070-83
pubmed: 10653820
Microbiology (Reading). 2000 Oct;146 ( Pt 10):2395-2407
pubmed: 11021916
Lupus. 1998;7(8):524-9
pubmed: 9863893
PLoS One. 2011;6(12):e28526
pubmed: 22174830
J Am Chem Soc. 2013 Jan 23;135(3):1117-23
pubmed: 23311576
Biochemistry (Mosc). 2004 Jun;69(6):587-601
pubmed: 15236597
J Biomol Struct Dyn. 1989 Apr;6(5):899-906
pubmed: 2590508
Am J Respir Cell Mol Biol. 2012 Jul;47(1):80-6
pubmed: 22343221
BMC Microbiol. 2008 Oct 08;8:173
pubmed: 18842140
Mol Microbiol. 2010 Nov;78(3):589-606
pubmed: 20969646
Nat Rev Microbiol. 2017 Dec;15(12):740-755
pubmed: 28944770
J Am Chem Soc. 2011 Feb 2;133(4):668-71
pubmed: 21171590
J Biomol Struct Dyn. 1988 Jun;5(6):1187-207
pubmed: 3271507
Biochem Mol Biol Int. 1997 May;41(6):1227-35
pubmed: 9161718
Biochimie. 1991 Feb-Mar;73(2-3):257-67
pubmed: 1653033
Nat Rev Genet. 2003 Jul;4(7):566-72
pubmed: 12838348
J Bacteriol. 2005 Jul;187(13):4627-36
pubmed: 15968074
Nucleic Acids Res. 1978 Oct;5(10):3643-63
pubmed: 724497
Microbiologyopen. 2018 Jun;7(3):e00563
pubmed: 29230970
Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16666-71
pubmed: 12486233
Nucleic Acids Res. 2016 Jun 20;44(11):e101
pubmed: 26896804
Nucleic Acids Res. 2009 Apr;37(6):1713-25
pubmed: 19190094
Curr Issues Mol Biol. 2011;13(1):1-12
pubmed: 20484776
Curr Opin Struct Biol. 2004 Feb;14(1):28-35
pubmed: 15102446
Genomics. 2009 Apr;93(4):383-91
pubmed: 19103278
J Mol Biol. 1972 Jun 28;67(3):375-96
pubmed: 5045303
Nucleic Acids Res. 2015 Feb 27;43(4):2282-92
pubmed: 25670677
Proc Natl Acad Sci U S A. 2017 Aug 8;114(32):E6632-E6641
pubmed: 28696280
J Bacteriol. 2016 Sep 09;198(19):2619-30
pubmed: 27044626
Mucosal Immunol. 2011 Jul;4(4):456-67
pubmed: 21326197
EMBO J. 1985 Dec 30;4(13B):3655-60
pubmed: 4092691
Cancer Res. 2013 Jan 15;73(2):736-44
pubmed: 23135915
Mucosal Immunol. 2011 Nov;4(6):625-37
pubmed: 21716265
NPJ Biofilms Microbiomes. 2021 Mar 19;7(1):27
pubmed: 33741996
Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2677-82
pubmed: 16473937
Science. 2004 Mar 5;303(5663):1532-5
pubmed: 15001782
J Biol Chem. 2000 Sep 1;275(35):26828-33
pubmed: 10843996
Nature. 2016 Dec 1;540(7631):129-133
pubmed: 27819682
Mol Biochem Parasitol. 1990 Mar;39(2):275-8
pubmed: 2320060
Cell. 1996 Dec 27;87(7):1295-306
pubmed: 8980235
PLoS Pathog. 2016 Jun 23;12(6):e1005686
pubmed: 27336156
Pathog Dis. 2020 Mar 1;78(2):
pubmed: 32196074
J Biol Chem. 1991 Apr 5;266(10):6137-41
pubmed: 1848849
Mol Microbiol. 2015 Jun;96(6):1119-35
pubmed: 25757804
J Mol Biol. 1988 May 20;201(2):463-7
pubmed: 3418706
Infect Immun. 2008 Jul;76(7):3337-45
pubmed: 18411285
Biochemistry. 2019 Apr 16;58(15):1963-1974
pubmed: 30950607
Science. 2002 Feb 22;295(5559):1487
pubmed: 11859186
mSphere. 2020 May 27;5(3):
pubmed: 32461275
EMBO J. 2000 Dec 1;19(23):6527-35
pubmed: 11101525
Mol Oral Microbiol. 2017 Apr;32(2):118-130
pubmed: 26988714
Thromb Haemost. 2018 Jul;118(7):1167-1175
pubmed: 29874690
Biofilm. 2020 Nov 18;2:100039
pubmed: 33447823
Proc Natl Acad Sci U S A. 1988 Oct;85(19):7069-73
pubmed: 3050986
Proc Natl Acad Sci U S A. 1983 Apr;80(7):1821-5
pubmed: 6572943
Am J Respir Cell Mol Biol. 2017 Apr;56(4):423-431
pubmed: 27854516
Nucleic Acids Res. 2016 Aug 19;44(14):6574-82
pubmed: 27387283
Nat Rev Microbiol. 2010 Sep;8(9):623-33
pubmed: 20676145
Sci Rep. 2018 Jun 26;8(1):9691
pubmed: 29946126
Infect Immun. 2001 Jul;69(7):4572-9
pubmed: 11402001
J Biol Chem. 2016 Jun 10;291(24):12538-12546
pubmed: 27129225
J Clin Invest. 2021 Aug 16;131(16):
pubmed: 34396989
Infect Dis Clin North Am. 2001 Jun;15(2):335-61, vii
pubmed: 11447699
Trends Immunol. 2018 Feb;39(2):123-134
pubmed: 29236673
Mol Microbiol. 2006 Mar;59(6):1831-47
pubmed: 16553887
J Cyst Fibros. 2013 Jul;12(4):384-9
pubmed: 23168017
Nucleic Acids Res. 1983 Dec 10;11(23):8485-94
pubmed: 6672770
EMBO J. 1991 Mar;10(3):687-96
pubmed: 2001682
J Innate Immun. 2014;6(6):765-79
pubmed: 24862346
Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2259-63
pubmed: 2006166
J Antibiot (Tokyo). 2012 Feb;65(2):73-7
pubmed: 22167157
Cell. 2020 Aug 20;182(4):919-932.e19
pubmed: 32763156
Mol Phylogenet Evol. 2017 Feb;107:356-366
pubmed: 27894997
Proc Natl Acad Sci U S A. 1985 Nov;82(22):7595-8
pubmed: 3865181
J Am Chem Soc. 2019 May 15;141(19):7758-7764
pubmed: 30844265
Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12759-64
pubmed: 16126896
Biochem Biophys Res Commun. 2017 Jan 22;482(4):916-921
pubmed: 27890616
DNA Res. 2016 Oct 1;23(5):477-486
pubmed: 27374614
Front Immunol. 2020 Feb 04;11:97
pubmed: 32117251
Mycoses. 2012 Jan;55(1):80-5
pubmed: 21668524
Nature. 1986 Jun 5-11;321(6070):620-5
pubmed: 3713845
Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):6974-9
pubmed: 12777633
Molecules. 2018 Oct 24;23(11):
pubmed: 30355979
Nucleic Acids Res. 2018 May 4;46(8):4129-4137
pubmed: 29584891
J Chromatogr A. 1996 Sep 13;744(1-2):285-94
pubmed: 8843677
Cell. 1982 Dec;31(2 Pt 1):309-18
pubmed: 7159926
Nucleic Acids Res. 2017 Feb 28;45(4):1925-1945
pubmed: 28082391
EBioMedicine. 2016 Aug;10:33-44
pubmed: 27342872

Auteurs

John R Buzzo (JR)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Aishwarya Devaraj (A)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Erin S Gloag (ES)

Department of Orthopedics, Ohio State University, Columbus, OH 43210, USA.

Joseph A Jurcisek (JA)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Frank Robledo-Avila (F)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Theresa Kesler (T)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Kathryn Wilbanks (K)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Lauren Mashburn-Warren (L)

The Steve and Cindy Rasmussen Institute for Genomic Medicine, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Sabarathnam Balu (S)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Joseph Wickham (J)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Laura A Novotny (LA)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA.

Paul Stoodley (P)

Department of Orthopedics, Ohio State University, Columbus, OH 43210, USA; Department of Microbial Infection and Immunity, Ohio State University, Columbus, OH 43210, USA; National Centre for Advanced Tribology at Southampton, University of Southampton, Southampton S017 1BJ, UK.

Lauren O Bakaletz (LO)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA; Department of Pediatrics, College of Medicine, Ohio State University, Columbus, OH 43210, USA. Electronic address: lauren.bakaletz@nationwidechildrens.org.

Steven D Goodman (SD)

Center for Microbial Pathogenesis, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH 43205, USA; Department of Pediatrics, College of Medicine, Ohio State University, Columbus, OH 43210, USA. Electronic address: steven.goodman@nationwidechildrens.org.

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