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Molecular and cellular insight into Escherichia coli SslE and its role during biofilm maturation

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Paula Corsini Madeira, Sunjun Wang, Saima Rehman, Katherine Fenn, Amin Sagar, Slobadan Sirovica, Leanne Cleaver, Charlotte Edwards-Gayle, Giulia Mastroianni, Benjamin James Dorgan, Lee Sewell, Steven Lynham, Dinu Iuga, W. Trents Franks, James Jarvis, Guy Carpenter, Michael Curtis, Pau Bernado, Vidya Darbari, James Garnett

Original languageEnglish
Article number9
Journalnpj Biofilms and Microbiomes
Volume8
Issue number1
DOIs
Accepted/In press31 Jan 2022
PublishedDec 2022

Bibliographical note

Funding Information: P.C. was supported by the Academy of Medical Sciences and Wellcome Trust (SBF002/1150) and S.R. was supported by the Medical Research Council (MR/R017662/1), awarded to J.A.G. S.W. and B.D. were supported by China Scholarship Council and Biotechnology and Biological Sciences Research Council studentships, respectively, awarded to J.A.G. and M.A.C. L.S. was supported by the Leverhulme Trust (RPG-2017-222), awarded to J.A.G. K.F. was supported by a PhD studentship from Queen Mary University of London and V.C.D. was supported by a start-up grant from Queen Mary University of London. This work was also supported by the Labex EpiGenMed, an « Investissements d’avenir » program (ANR-10-LABX-12-01) awarded to P.B. The C.B.S. is a member of France-BioImaging (FBI) and the French Infrastructure for Integrated Structural Biology (FRISBI), 2 national infrastructures supported by the French National Research Agency (ANR-10-INBS-04-01 and ANR-10-INBS-05, respectively). We thank the beamline scientists at B21 of the Diamond Light Source, United Kingdom. This work was also supported by the Francis Crick Institute through provision of access to the MRC Biomedical NMR centre. The Francis Crick Institute receives its core funding from Cancer Research United Kingdom (FC001029), the United Kingdom Medical Research Council (FC001029), and the Wellcome Trust (FC001029). As this research was funded in part by the Wellcome Trust, for the purpose of open access, the authors have applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. We also thank the Centre for Biomolecular Spectroscopy at King’s College London for additional NMR access, funded by the Wellcome Trust and British Heart Foundation (ref. 202767/Z/16/Z and IG/16/2/32273, respectively). The UK 850 MHz solid-state NMR Facility used in this research was funded by EPSRC and BBSRC (contract reference EP/T015063/1), as well as the University of Warwick including via part funding through Birmingham Science City Advanced Materials Projects 1 and 2 supported by Advantage West Midlands (AWM) and the European Regional Development Fund (ERDF). We would like to thank Prof. Cynthia Whitchurch (Quadram Institute, UK) for providing the EPEC E2348/69 ΔsslE strain and Prof. Jorge Girón (Benemérita Universidad Autónoma de Puebla, Mexico) for providing the EPEC E2348/69 wild-type, ΔcsgA and ΔcsgA /ΔbcsA strains. Cellulose discs were gifted by Prof. Tom Ellis and Kenneth T. Walker (Imperial College London, UK). Funding Information: P.C. was supported by the Academy of Medical Sciences and Wellcome Trust (SBF002/1150) and S.R. was supported by the Medical Research Council (MR/R017662/1), awarded to J.A.G. S.W. and B.D. were supported by China Scholarship Council and Biotechnology and Biological Sciences Research Council studentships, respectively, awarded to J.A.G. and M.A.C. L.S. was supported by the Leverhulme Trust (RPG-2017-222), awarded to J.A.G. K.F. was supported by a PhD studentship from Queen Mary University of London and V.C.D. was supported by a start-up grant from Queen Mary University of London. This work was also supported by the Labex EpiGenMed, an « Investissements d’avenir » program (ANR-10-LABX-12-01) awarded to P.B. The C.B.S. is a member of France-BioImaging (FBI) and the French Infrastructure for Integrated Structural Biology (FRISBI), 2 national infrastructures supported by the French National Research Agency (ANR-10-INBS-04-01 and ANR-10-INBS-05, respectively). We thank the beamline scientists at B21 of the Diamond Light Source, United Kingdom. This work was also supported by the Francis Crick Institute through provision of access to the MRC Biomedical NMR centre. The Francis Crick Institute receives its core funding from Cancer Research United Kingdom (FC001029), the United Kingdom Medical Research Council (FC001029), and the Wellcome Trust (FC001029). As this research was funded in part by the Wellcome Trust, for the purpose of open access, the authors have applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. We also thank the Centre for Biomolecular Spectroscopy at King’s College London for additional NMR access, funded by the Wellcome Trust and British Heart Foundation (ref. 202767/Z/16/Z and IG/16/2/32273, respectively). The UK 850 MHz solid-state NMR Facility used in this research was funded by EPSRC and BBSRC (contract reference EP/T015063/1), as well as the University of Warwick including via part funding through Birmingham Science City Advanced Materials Projects 1 and 2 supported by Advantage West Midlands (AWM) and the European Regional Development Fund (ERDF). We would like to thank Prof. Cynthia Whitchurch (Quadram Institute, UK) for providing the EPEC E2348/69 ΔsslE strain and Prof. Jorge Girón (Benemérita Universidad Autónoma de Puebla, Mexico) for providing the EPEC E2348/69 wild-type, ΔcsgA and ΔcsgA/ΔbcsA strains. Cellulose discs were gifted by Prof. Tom Ellis and Kenneth T. Walker (Imperial College London, UK). Publisher Copyright: © 2022, The Author(s).

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Abstract

Escherichia coli is a Gram-negative bacterium that colonises the human intestine and virulent strains can cause severe diarrhoeal and extraintestinal diseases. The protein SslE is secreted by a range of pathogenic and commensal E. coli strains. It can degrade mucins in the intestine, promotes biofilm maturation and it is a major determinant of infection in virulent strains, although how it carries out these functions is not well understood. Here, we examine SslE from the commensal E. coli Waksman and BL21 (DE3) strains and the enterotoxigenic H10407 and enteropathogenic E2348/69 strains. We reveal that SslE has a unique and dynamic structure in solution and in response to acidification within mature biofilms it can form a unique aggregate with amyloid-like properties. Furthermore, we show that both SslE monomers and aggregates bind DNA in vitro and co-localise with extracellular DNA (eDNA) in mature biofilms, and SslE aggregates may also associate with cellulose under certain conditions. Our results suggest that interactions between SslE and eDNA are important for biofilm maturation in many E. coli strains and SslE may also be a factor that drives biofilm formation in other SslE-secreting bacteria.

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