Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical Materials

Medical device-associated staphylococcal infections are a common and challenging problem. However, detailed knowledge of staphylococcal biofilm dynamics on clinically relevant surfaces is still limited. In the present study, biofilm formation of the <i>Staphylococcus</i><i> </i&...

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Main Authors: Anna K. Hiltunen, Kirsi Savijoki, Tuula A. Nyman, Ilkka Miettinen, Petri Ihalainen, Jouko Peltonen, Adyary Fallarero
Format: Article
Language:English
Published: MDPI AG 2019-11-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/7/12/584
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spelling doaj-eab15193a498470f9544c818175c9bd92020-11-25T02:00:17ZengMDPI AGMicroorganisms2076-26072019-11-0171258410.3390/microorganisms7120584microorganisms7120584Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical MaterialsAnna K. Hiltunen0Kirsi Savijoki1Tuula A. Nyman2Ilkka Miettinen3Petri Ihalainen4Jouko Peltonen5Adyary Fallarero6Pharmaceutical Design and Discovery (PharmDD) Group, Pharmaceutical Biology, Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Viikinkaari 5, 00014 Helsinki, FinlandPharmaceutical Design and Discovery (PharmDD) Group, Pharmaceutical Biology, Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Viikinkaari 5, 00014 Helsinki, FinlandDepartment of Immunology, Institute of Clinical Medicine, University of Oslo and Rikshospitalet Oslo, 0372 Oslo, NorwayPharmaceutical Design and Discovery (PharmDD) Group, Pharmaceutical Biology, Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Viikinkaari 5, 00014 Helsinki, FinlandLaboratory of Physical Chemistry, Åbo Akademi University, Porthaninkatu 3-5, 20500 Turku, FinlandLaboratory of Physical Chemistry, Åbo Akademi University, Porthaninkatu 3-5, 20500 Turku, FinlandPharmaceutical Design and Discovery (PharmDD) Group, Pharmaceutical Biology, Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Viikinkaari 5, 00014 Helsinki, FinlandMedical device-associated staphylococcal infections are a common and challenging problem. However, detailed knowledge of staphylococcal biofilm dynamics on clinically relevant surfaces is still limited. In the present study, biofilm formation of the <i>Staphylococcus</i><i> </i><i>aureus</i> ATCC 25923 strain was studied on clinically relevant materials&#8212;borosilicate glass, plexiglass, hydroxyapatite, titanium and polystyrene&#8212;at 18, 42 and 66 h. Materials with the highest surface roughness and porosity (hydroxyapatite and plexiglass) did not promote biofilm formation as efficiently as some other selected materials. Matrix-associated poly-<i>N</i>-acetyl-&#946;-(1-6)-glucosamine (PNAG) was considered important in young (18 h) biofilms, whereas proteins appeared to play a more important role at later stages of biofilm development. A total of 460 proteins were identified from biofilm matrices formed on the indicated materials and time points&#8212;from which, 66 proteins were proposed to form the core surfaceome. At 18 h, the appearance of several r-proteins and glycolytic adhesive moonlighters, possibly via an autolysin (AtlA)-mediated release, was demonstrated in all materials, whereas classical surface adhesins, resistance- and virulence-associated proteins displayed greater variation in their abundances depending on the used material. Hydroxyapatite-associated biofilms were more susceptible to antibiotics than biofilms formed on titanium, but no clear correlation between the tolerance and biofilm age was observed. Thus, other factors, possibly the adhesive moonlighters, could have contributed to the observed chemotolerant phenotype. In addition, a protein-dependent matrix network was observed to be already well-established at the 18 h time point. To the best of our knowledge, this is among the first studies shedding light into matrix-associated surfaceomes of S. aureus biofilms grown on different clinically relevant materials and at different time points.https://www.mdpi.com/2076-2607/7/12/584staphylococcus aureusbiofilm matrixclinical materialexopolysaccharideproteinssurfaceome
collection DOAJ
language English
format Article
sources DOAJ
author Anna K. Hiltunen
Kirsi Savijoki
Tuula A. Nyman
Ilkka Miettinen
Petri Ihalainen
Jouko Peltonen
Adyary Fallarero
spellingShingle Anna K. Hiltunen
Kirsi Savijoki
Tuula A. Nyman
Ilkka Miettinen
Petri Ihalainen
Jouko Peltonen
Adyary Fallarero
Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical Materials
Microorganisms
staphylococcus aureus
biofilm matrix
clinical material
exopolysaccharide
proteins
surfaceome
author_facet Anna K. Hiltunen
Kirsi Savijoki
Tuula A. Nyman
Ilkka Miettinen
Petri Ihalainen
Jouko Peltonen
Adyary Fallarero
author_sort Anna K. Hiltunen
title Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical Materials
title_short Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical Materials
title_full Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical Materials
title_fullStr Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical Materials
title_full_unstemmed Structural and Functional Dynamics of <i>Staphylococcus aureus</i> Biofilms and Biofilm Matrix Proteins on Different Clinical Materials
title_sort structural and functional dynamics of <i>staphylococcus aureus</i> biofilms and biofilm matrix proteins on different clinical materials
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2019-11-01
description Medical device-associated staphylococcal infections are a common and challenging problem. However, detailed knowledge of staphylococcal biofilm dynamics on clinically relevant surfaces is still limited. In the present study, biofilm formation of the <i>Staphylococcus</i><i> </i><i>aureus</i> ATCC 25923 strain was studied on clinically relevant materials&#8212;borosilicate glass, plexiglass, hydroxyapatite, titanium and polystyrene&#8212;at 18, 42 and 66 h. Materials with the highest surface roughness and porosity (hydroxyapatite and plexiglass) did not promote biofilm formation as efficiently as some other selected materials. Matrix-associated poly-<i>N</i>-acetyl-&#946;-(1-6)-glucosamine (PNAG) was considered important in young (18 h) biofilms, whereas proteins appeared to play a more important role at later stages of biofilm development. A total of 460 proteins were identified from biofilm matrices formed on the indicated materials and time points&#8212;from which, 66 proteins were proposed to form the core surfaceome. At 18 h, the appearance of several r-proteins and glycolytic adhesive moonlighters, possibly via an autolysin (AtlA)-mediated release, was demonstrated in all materials, whereas classical surface adhesins, resistance- and virulence-associated proteins displayed greater variation in their abundances depending on the used material. Hydroxyapatite-associated biofilms were more susceptible to antibiotics than biofilms formed on titanium, but no clear correlation between the tolerance and biofilm age was observed. Thus, other factors, possibly the adhesive moonlighters, could have contributed to the observed chemotolerant phenotype. In addition, a protein-dependent matrix network was observed to be already well-established at the 18 h time point. To the best of our knowledge, this is among the first studies shedding light into matrix-associated surfaceomes of S. aureus biofilms grown on different clinically relevant materials and at different time points.
topic staphylococcus aureus
biofilm matrix
clinical material
exopolysaccharide
proteins
surfaceome
url https://www.mdpi.com/2076-2607/7/12/584
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