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Identification of novel Staphylococcus aureus core and accessory virulence patterns in chronic rhinosinusitis

Identification of novel Staphylococcus aureus core and accessory virulence patterns in chronic rhinosinusitis
Identification of novel Staphylococcus aureus core and accessory virulence patterns in chronic rhinosinusitis

Staphylococcus aureus (S. aureus) colonizes the nasal cavities of both healthy individuals and patients with chronic rhinosinusitis (CRS) with (CRSwNP) and without (CRSsNP) nasal polyps. Treatment-resistant S. aureus biofilms and intracellular persistence are common in CRS patients, requiring the expression of specific virulence factor genes to transition into these forms. We hypothesized that S. aureus isolates from non-diseased controls, CRSsNP patients, and CRSwNP patients would exhibit distinct virulence factor patterns contributing to persistence and intracellular survival in CRS patients. Nasal swabs from seventy-seven individuals yielded S. aureus cultures in eight non-diseased controls, eight CRSsNP patients, and five CRSwNP patients. Whole-genome sequencing analyzed stress, antimicrobial resistance, and virulence genes, including plasmids and prophages. Four virulence factor gene patterns emerged: a core set (hlgA, icaC, hlgB, hlgC, hld, and aur) present in all isolates, and accessory sets, including the enterotoxin gene cluster (seo, sem, seu, sei, and sen) and a partial/complete invasive virulence factor set (splE, splA, splB, lukE, and lukD) (p = 0.001). CRSwNP isolates exhibited incomplete carriage of the core set, with frequent loss of scn, icaC, and hlgA (p < 0.05). These findings suggest that S. aureus has clusters of virulence factors that may act in concert to support the survival and persistence of the bacteria, resulting in enhanced pathogenicity. This may manifest clinically with resistant disease and refractoriness to antibiotics.

Adult, Aged, Bacterial Proteins/genetics, Biofilms, Chronic Disease, Female, Humans, Male, Middle Aged, Rhinitis/microbiology, Rhinosinusitis, Sinusitis/microbiology, Staphylococcal Infections/microbiology, Staphylococcus aureus/genetics, Virulence Factors/genetics, Virulence/genetics, quorum sensing, virulence factors, chronic rhinosinusitis, biofilms, Staphylococcus aureus
1422-0067
Goldie, Simon P.
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Lau, Laurie C.
2af8045d-6162-4939-aba7-28dd2f60f6a8
Jones, Huw A.S.
5d258f82-5345-4326-bdea-8e00681c4f1f
Harries, Philip G.
df33be64-b580-4fdf-ac4d-4c842b55d753
Walls, Andrew F.
aaa7e455-0562-4b4c-94f5-ec29c74b1bfe
Salib, Rami J.
d6fde1c1-5b5e-43f7-ae1c-42cce6a0c9fc
Goldie, Simon P.
0bf2f8c9-290b-403f-bf52-5602708810e9
Lau, Laurie C.
2af8045d-6162-4939-aba7-28dd2f60f6a8
Jones, Huw A.S.
5d258f82-5345-4326-bdea-8e00681c4f1f
Harries, Philip G.
df33be64-b580-4fdf-ac4d-4c842b55d753
Walls, Andrew F.
aaa7e455-0562-4b4c-94f5-ec29c74b1bfe
Salib, Rami J.
d6fde1c1-5b5e-43f7-ae1c-42cce6a0c9fc

Goldie, Simon P., Lau, Laurie C., Jones, Huw A.S., Harries, Philip G., Walls, Andrew F. and Salib, Rami J. (2025) Identification of novel Staphylococcus aureus core and accessory virulence patterns in chronic rhinosinusitis. International Journal of Molecular Sciences, 26 (8), [3711]. (doi:10.3390/ijms26083711).

Record type: Article

Abstract

Staphylococcus aureus (S. aureus) colonizes the nasal cavities of both healthy individuals and patients with chronic rhinosinusitis (CRS) with (CRSwNP) and without (CRSsNP) nasal polyps. Treatment-resistant S. aureus biofilms and intracellular persistence are common in CRS patients, requiring the expression of specific virulence factor genes to transition into these forms. We hypothesized that S. aureus isolates from non-diseased controls, CRSsNP patients, and CRSwNP patients would exhibit distinct virulence factor patterns contributing to persistence and intracellular survival in CRS patients. Nasal swabs from seventy-seven individuals yielded S. aureus cultures in eight non-diseased controls, eight CRSsNP patients, and five CRSwNP patients. Whole-genome sequencing analyzed stress, antimicrobial resistance, and virulence genes, including plasmids and prophages. Four virulence factor gene patterns emerged: a core set (hlgA, icaC, hlgB, hlgC, hld, and aur) present in all isolates, and accessory sets, including the enterotoxin gene cluster (seo, sem, seu, sei, and sen) and a partial/complete invasive virulence factor set (splE, splA, splB, lukE, and lukD) (p = 0.001). CRSwNP isolates exhibited incomplete carriage of the core set, with frequent loss of scn, icaC, and hlgA (p < 0.05). These findings suggest that S. aureus has clusters of virulence factors that may act in concert to support the survival and persistence of the bacteria, resulting in enhanced pathogenicity. This may manifest clinically with resistant disease and refractoriness to antibiotics.

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Accepted/In Press date: 11 April 2025
Published date: 14 April 2025
Keywords: Adult, Aged, Bacterial Proteins/genetics, Biofilms, Chronic Disease, Female, Humans, Male, Middle Aged, Rhinitis/microbiology, Rhinosinusitis, Sinusitis/microbiology, Staphylococcal Infections/microbiology, Staphylococcus aureus/genetics, Virulence Factors/genetics, Virulence/genetics, quorum sensing, virulence factors, chronic rhinosinusitis, biofilms, Staphylococcus aureus

Identifiers

Local EPrints ID: 502937
URI: http://eprints.soton.ac.uk/id/eprint/502937
ISSN: 1422-0067
PURE UUID: 9266f50d-be69-4015-9bef-21f166756d27
ORCID for Simon P. Goldie: ORCID iD orcid.org/0000-0002-3912-9026
ORCID for Andrew F. Walls: ORCID iD orcid.org/0000-0003-4803-4595
ORCID for Rami J. Salib: ORCID iD orcid.org/0000-0002-6753-7844

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Date deposited: 14 Jul 2025 16:39
Last modified: 11 Sep 2025 02:07

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Contributors

Author: Simon P. Goldie ORCID iD
Author: Laurie C. Lau
Author: Huw A.S. Jones
Author: Philip G. Harries
Author: Andrew F. Walls ORCID iD
Author: Rami J. Salib ORCID iD

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