Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic Acid

Biofilms are typically studied in bacterial media that allow the study of important properties such as bacterial growth. However, the results obtained in such media cannot take into account the bacterial localization/clustering caused by bacteria–protein interactions in vivo and the accompanying alt...

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Main Authors: Samantha Knott, Dylan Curry, Neil Zhao, Pallavi Metgud, Sana S. Dastgheyb, Caroline Purtill, Marc Harwood, Antonia F. Chen, Thomas P. Schaer, Michael Otto, Noreen J. Hickok
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.655873/full
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author Samantha Knott
Dylan Curry
Neil Zhao
Pallavi Metgud
Sana S. Dastgheyb
Caroline Purtill
Marc Harwood
Antonia F. Chen
Thomas P. Schaer
Michael Otto
Noreen J. Hickok
author_facet Samantha Knott
Dylan Curry
Neil Zhao
Pallavi Metgud
Sana S. Dastgheyb
Caroline Purtill
Marc Harwood
Antonia F. Chen
Thomas P. Schaer
Michael Otto
Noreen J. Hickok
author_sort Samantha Knott
collection DOAJ
description Biofilms are typically studied in bacterial media that allow the study of important properties such as bacterial growth. However, the results obtained in such media cannot take into account the bacterial localization/clustering caused by bacteria–protein interactions in vivo and the accompanying alterations in phenotype, virulence factor production, and ultimately antibiotic tolerance. We and others have reported that methicillin-resistant or methicillin-susceptible Staphylococcus aureus (MRSA or MSSA, respectively) and other pathogens assemble a proteinaceous matrix in synovial fluid. This proteinaceous bacterial aggregate is coated by a polysaccharide matrix as is characteristic of biofilms. In this study, we identify proteins important for this aggregation and determine the concentration ranges of these proteins that can reproduce bacterial aggregation. We then test this protein combination for its ability to cause marked aggregation, antibacterial tolerance, preservation of morphology, and expression of the phenol-soluble modulin (PSM) virulence factors. In the process, we create a viscous fluid that models bacterial behavior in synovial fluid. We suggest that our findings and, by extension, use of this fluid can help to better model bacterial behavior of new antimicrobial therapies, as well as serve as a starting point to study host protein–bacteria interactions characteristic of physiological fluids.
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spelling doaj.art-4b015f02d5e642f2a8431da3e26628af2022-12-21T19:42:32ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-04-011210.3389/fmicb.2021.655873655873Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic AcidSamantha Knott0Dylan Curry1Neil Zhao2Pallavi Metgud3Sana S. Dastgheyb4Caroline Purtill5Marc Harwood6Antonia F. Chen7Thomas P. Schaer8Michael Otto9Noreen J. Hickok10Department of Orthopaedic Surgery, Sidney Kimmel Medical College of Thomas Jefferson University, Philadelphia, PA, United StatesDepartment of Orthopaedic Surgery, Sidney Kimmel Medical College of Thomas Jefferson University, Philadelphia, PA, United StatesDepartment of Orthopaedic Surgery, Sidney Kimmel Medical College of Thomas Jefferson University, Philadelphia, PA, United StatesDepartment of Orthopaedic Surgery, Sidney Kimmel Medical College of Thomas Jefferson University, Philadelphia, PA, United StatesDepartment of Orthopaedic Surgery, Sidney Kimmel Medical College of Thomas Jefferson University, Philadelphia, PA, United StatesDepartment of Orthopaedic Surgery, Sidney Kimmel Medical College of Thomas Jefferson University, Philadelphia, PA, United StatesRothman Orthopaedic Institute, Philadelphia, PA, United StatesDepartment of Orthopaedic Surgery, Brigham and Women’s Hospital, Boston, PA, United StatesDepartment of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA, United StatesPathogen Molecular Genetics Section, Laboratory of Human Bacterial Pathogenesis, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, United StatesDepartment of Orthopaedic Surgery, Sidney Kimmel Medical College of Thomas Jefferson University, Philadelphia, PA, United StatesBiofilms are typically studied in bacterial media that allow the study of important properties such as bacterial growth. However, the results obtained in such media cannot take into account the bacterial localization/clustering caused by bacteria–protein interactions in vivo and the accompanying alterations in phenotype, virulence factor production, and ultimately antibiotic tolerance. We and others have reported that methicillin-resistant or methicillin-susceptible Staphylococcus aureus (MRSA or MSSA, respectively) and other pathogens assemble a proteinaceous matrix in synovial fluid. This proteinaceous bacterial aggregate is coated by a polysaccharide matrix as is characteristic of biofilms. In this study, we identify proteins important for this aggregation and determine the concentration ranges of these proteins that can reproduce bacterial aggregation. We then test this protein combination for its ability to cause marked aggregation, antibacterial tolerance, preservation of morphology, and expression of the phenol-soluble modulin (PSM) virulence factors. In the process, we create a viscous fluid that models bacterial behavior in synovial fluid. We suggest that our findings and, by extension, use of this fluid can help to better model bacterial behavior of new antimicrobial therapies, as well as serve as a starting point to study host protein–bacteria interactions characteristic of physiological fluids.https://www.frontiersin.org/articles/10.3389/fmicb.2021.655873/fullStaphylococcus aureusbiofilmsynovial fluidantibiotic tolerancevirulence factors
spellingShingle Samantha Knott
Dylan Curry
Neil Zhao
Pallavi Metgud
Sana S. Dastgheyb
Caroline Purtill
Marc Harwood
Antonia F. Chen
Thomas P. Schaer
Michael Otto
Noreen J. Hickok
Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic Acid
Frontiers in Microbiology
Staphylococcus aureus
biofilm
synovial fluid
antibiotic tolerance
virulence factors
title Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic Acid
title_full Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic Acid
title_fullStr Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic Acid
title_full_unstemmed Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic Acid
title_short Staphylococcus aureus Floating Biofilm Formation and Phenotype in Synovial Fluid Depends on Albumin, Fibrinogen, and Hyaluronic Acid
title_sort staphylococcus aureus floating biofilm formation and phenotype in synovial fluid depends on albumin fibrinogen and hyaluronic acid
topic Staphylococcus aureus
biofilm
synovial fluid
antibiotic tolerance
virulence factors
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.655873/full
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