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Rapid aggregation of Staphylococcus aureus in synovial fluid is influenced by synovial fluid concentration, viscosity, and fluid dynamics-with evidence of polymer bridging

Rapid aggregation of Staphylococcus aureus in synovial fluid is influenced by synovial fluid concentration, viscosity, and fluid dynamics-with evidence of polymer bridging
Rapid aggregation of Staphylococcus aureus in synovial fluid is influenced by synovial fluid concentration, viscosity, and fluid dynamics-with evidence of polymer bridging
Early bacterial survival in the post-surgical joint is still a mystery. Recently, synovial fluid-induced aggregation was proposed as a potential mechanism of bacterial protection upon entry into the joint. As synovial fluid is secreted back into the joint cavity following surgery, rapid fluctuations in synovial fluid concentration, composition, and viscosity occur. These changes, along with fluid movement from post-operative joint motion, will modify the environment and potentially affect the kinetics of aggregate formation. Through this work, we sought to evaluate the influence of exposure time, synovial fluid concentration, viscosity, and fluid dynamics on aggregation. Furthermore, we aimed to elucidate the primary mechanism of aggregate formation by assessing the interaction of bacterial adhesins with synovial fluid polymer, fibrinogen. Following incubation in each simulated post-operative joint condition, the aggregates were imaged using confocal microscopy. Our analysis revealed the formation of two distinct aggregate phenotypes dependent on whether the incubation was conducted under static or dynamic conditions. Using a surface adhesin mutant, we have narrowed down the genetic determinants for synovial fluid aggregate formation and identified essential host polymers required. We report here that synovial fluid-induced aggregation is influenced by various changes specific to the post-surgical joint environment. While we now have evidence that select synovial fluid polymers facilitate bridging aggregation through essential bacterial adhesins, we suspect that their utility is limited by the increasing viscosity under static conditions. Furthermore, dynamic fluid movement recovers the ability of the bacteria with present surface proteins to aggregate under high viscosity conditions, yielding large, globular aggregates.
Surgical Joint, Synovial Fluid, Aggregation, S. aureus, Orthopaedics
2150-7511
Staats, Amelia M.
67926f6c-53d4-49bb-800c-6e850aaafb0b
Burback, Peter W.
4ac12008-483e-48de-aafa-7485d7f2a39e
Schwieters, Andrew
1fa39257-b1a6-4d40-b4f5-2ae4a4f86d27
Li, Daniel
216db1e1-42cd-487c-9f31-65321d6c4c66
Sullivan, Anne
2fc4e087-c92c-405d-9071-18d5873b4cbd
Horswill, Alexander R.
7590c3a8-9933-4300-abed-e1b94faafaa6
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Staats, Amelia M.
67926f6c-53d4-49bb-800c-6e850aaafb0b
Burback, Peter W.
4ac12008-483e-48de-aafa-7485d7f2a39e
Schwieters, Andrew
1fa39257-b1a6-4d40-b4f5-2ae4a4f86d27
Li, Daniel
216db1e1-42cd-487c-9f31-65321d6c4c66
Sullivan, Anne
2fc4e087-c92c-405d-9071-18d5873b4cbd
Horswill, Alexander R.
7590c3a8-9933-4300-abed-e1b94faafaa6
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f

Staats, Amelia M., Burback, Peter W., Schwieters, Andrew, Li, Daniel, Sullivan, Anne, Horswill, Alexander R. and Stoodley, Paul (2022) Rapid aggregation of Staphylococcus aureus in synovial fluid is influenced by synovial fluid concentration, viscosity, and fluid dynamics-with evidence of polymer bridging. mBio. (In Press)

Record type: Article

Abstract

Early bacterial survival in the post-surgical joint is still a mystery. Recently, synovial fluid-induced aggregation was proposed as a potential mechanism of bacterial protection upon entry into the joint. As synovial fluid is secreted back into the joint cavity following surgery, rapid fluctuations in synovial fluid concentration, composition, and viscosity occur. These changes, along with fluid movement from post-operative joint motion, will modify the environment and potentially affect the kinetics of aggregate formation. Through this work, we sought to evaluate the influence of exposure time, synovial fluid concentration, viscosity, and fluid dynamics on aggregation. Furthermore, we aimed to elucidate the primary mechanism of aggregate formation by assessing the interaction of bacterial adhesins with synovial fluid polymer, fibrinogen. Following incubation in each simulated post-operative joint condition, the aggregates were imaged using confocal microscopy. Our analysis revealed the formation of two distinct aggregate phenotypes dependent on whether the incubation was conducted under static or dynamic conditions. Using a surface adhesin mutant, we have narrowed down the genetic determinants for synovial fluid aggregate formation and identified essential host polymers required. We report here that synovial fluid-induced aggregation is influenced by various changes specific to the post-surgical joint environment. While we now have evidence that select synovial fluid polymers facilitate bridging aggregation through essential bacterial adhesins, we suspect that their utility is limited by the increasing viscosity under static conditions. Furthermore, dynamic fluid movement recovers the ability of the bacteria with present surface proteins to aggregate under high viscosity conditions, yielding large, globular aggregates.

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mBio-V20-Manuscript 1 - Accepted Manuscript
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Accepted/In Press date: 8 February 2022
Keywords: Surgical Joint, Synovial Fluid, Aggregation, S. aureus, Orthopaedics

Identifiers

Local EPrints ID: 454943
URI: http://eprints.soton.ac.uk/id/eprint/454943
ISSN: 2150-7511
PURE UUID: d0c43f8d-4130-4593-84cb-84401a4d6ae7
ORCID for Paul Stoodley: ORCID iD orcid.org/0000-0001-6069-273X

Catalogue record

Date deposited: 02 Mar 2022 17:43
Last modified: 17 Mar 2024 03:18

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Contributors

Author: Amelia M. Staats
Author: Peter W. Burback
Author: Andrew Schwieters
Author: Daniel Li
Author: Anne Sullivan
Author: Alexander R. Horswill
Author: Paul Stoodley ORCID iD

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