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In vitro staphylococcal aggregate morphology and protection from antibiotics is dependent on distinct mechanisms arising from postsurgical joint components and fluid motion

In vitro staphylococcal aggregate morphology and protection from antibiotics is dependent on distinct mechanisms arising from postsurgical joint components and fluid motion
In vitro staphylococcal aggregate morphology and protection from antibiotics is dependent on distinct mechanisms arising from postsurgical joint components and fluid motion
Considerable progress has been made toward elucidating the mechanism of Staphylococcus aureus aggregation in synovial fluid. In this study, aggregate morphology was assessed following incubation in several simulated postsurgical joint conditions. Using fluorescently labeled synovial fluid polymers, we show that aggregation occurs through two distinct mechanisms: direct bridging between S. aureus cells and host fibrinogen, and an entropy-driven depletion mechanism facilitated by hyaluronic acid and albumin. By screening surface adhesin deficient mutants (clfA, clfB, fnbB, and fnbA), we identified the primary genetic determinant of aggregation in synovial fluid to be Clumping factor A. To characterize this bridging interaction, we employed an atomic force microscopy- based approach to quantify the binding affinity of either wild type S. aureus or the adhesin mutant to immobilized fibrinogen. Surprisingly, we found there to be cell-to-cell variability in the binding strength of the bacteria to immobilized fibrinogen. Super high resolution microscopy imaging revealed that fibrinogen binding to the cell wall is heterogeneously distributed at both the single cell and population level. Finally, we assessed the antibiotic tolerance of various aggregate morphologies arising from newly deciphered mechanisms of polymer-mediated synovial fluid-induced aggregation. The formation of macroscopic aggregates under shear, were highly tolerant of gentamicin, while smaller aggregates, formed under static conditions were susceptible. We hypothesize that aggregate formation in the joint cavity, in combination with shear, is mediated by both polymer-mediated aggregation mechanisms, with depletion forces enhancing the stability of essential bridging interactions.

in vitro, staphylococcal aggregate morphology, protection from antibiotics, postsurgical joint components, fluid motion
0021-9193
Staats, Amelia M.
67926f6c-53d4-49bb-800c-6e850aaafb0b
Burback, Peter W.
4ac12008-483e-48de-aafa-7485d7f2a39e
Casillas-Ituarte, Nadia N.
5cdcb4b1-6d70-4d65-aa00-a8466b398c63
Li, Daniel
6b3d9b08-53d8-4ed1-a47c-8567be975f4e
Hostetler, Michaela R.
5ffd5484-b315-4607-8f71-afc105670122
Sullivan, Anne
2fc4e087-c92c-405d-9071-18d5873b4cbd
Horswill, Alexander R.
7590c3a8-9933-4300-abed-e1b94faafaa6
Lower, Steven K.
b5d6cb17-c0de-4661-9a1a-24d29b12c39b
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Staats, Amelia M.
67926f6c-53d4-49bb-800c-6e850aaafb0b
Burback, Peter W.
4ac12008-483e-48de-aafa-7485d7f2a39e
Casillas-Ituarte, Nadia N.
5cdcb4b1-6d70-4d65-aa00-a8466b398c63
Li, Daniel
6b3d9b08-53d8-4ed1-a47c-8567be975f4e
Hostetler, Michaela R.
5ffd5484-b315-4607-8f71-afc105670122
Sullivan, Anne
2fc4e087-c92c-405d-9071-18d5873b4cbd
Horswill, Alexander R.
7590c3a8-9933-4300-abed-e1b94faafaa6
Lower, Steven K.
b5d6cb17-c0de-4661-9a1a-24d29b12c39b
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f

Staats, Amelia M., Burback, Peter W., Casillas-Ituarte, Nadia N., Li, Daniel, Hostetler, Michaela R., Sullivan, Anne, Horswill, Alexander R., Lower, Steven K. and Stoodley, Paul (2023) In vitro staphylococcal aggregate morphology and protection from antibiotics is dependent on distinct mechanisms arising from postsurgical joint components and fluid motion. Journal of Bacteriology. (In Press)

Record type: Article

Abstract

Considerable progress has been made toward elucidating the mechanism of Staphylococcus aureus aggregation in synovial fluid. In this study, aggregate morphology was assessed following incubation in several simulated postsurgical joint conditions. Using fluorescently labeled synovial fluid polymers, we show that aggregation occurs through two distinct mechanisms: direct bridging between S. aureus cells and host fibrinogen, and an entropy-driven depletion mechanism facilitated by hyaluronic acid and albumin. By screening surface adhesin deficient mutants (clfA, clfB, fnbB, and fnbA), we identified the primary genetic determinant of aggregation in synovial fluid to be Clumping factor A. To characterize this bridging interaction, we employed an atomic force microscopy- based approach to quantify the binding affinity of either wild type S. aureus or the adhesin mutant to immobilized fibrinogen. Surprisingly, we found there to be cell-to-cell variability in the binding strength of the bacteria to immobilized fibrinogen. Super high resolution microscopy imaging revealed that fibrinogen binding to the cell wall is heterogeneously distributed at both the single cell and population level. Finally, we assessed the antibiotic tolerance of various aggregate morphologies arising from newly deciphered mechanisms of polymer-mediated synovial fluid-induced aggregation. The formation of macroscopic aggregates under shear, were highly tolerant of gentamicin, while smaller aggregates, formed under static conditions were susceptible. We hypothesize that aggregate formation in the joint cavity, in combination with shear, is mediated by both polymer-mediated aggregation mechanisms, with depletion forces enhancing the stability of essential bridging interactions.

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Accepted/In Press date: 13 February 2023
Keywords: in vitro, staphylococcal aggregate morphology, protection from antibiotics, postsurgical joint components, fluid motion

Identifiers

Local EPrints ID: 475430
URI: http://eprints.soton.ac.uk/id/eprint/475430
ISSN: 0021-9193
PURE UUID: 56319330-8e8f-42d4-80e0-367c5d15e339
ORCID for Paul Stoodley: ORCID iD orcid.org/0000-0001-6069-273X

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Date deposited: 17 Mar 2023 17:38
Last modified: 17 Mar 2024 03:18

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Contributors

Author: Amelia M. Staats
Author: Peter W. Burback
Author: Nadia N. Casillas-Ituarte
Author: Daniel Li
Author: Michaela R. Hostetler
Author: Anne Sullivan
Author: Alexander R. Horswill
Author: Steven K. Lower
Author: Paul Stoodley ORCID iD

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