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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Frontiers Media S.A.
2021-04-01
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Series: | Frontiers in Microbiology |
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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. |
first_indexed | 2024-12-20T11:20:01Z |
format | Article |
id | doaj.art-4b015f02d5e642f2a8431da3e26628af |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-12-20T11:20:01Z |
publishDate | 2021-04-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Microbiology |
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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