Resistome, mobilome, and virulome explored in clinical isolates derived from acne patients in Egypt: unveiling unique traits of an emerging coagulase-negative Staphylococcus pathogen
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Date
2024-02
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Article
Publisher
Frontiers Media S.A.
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Frontiers in Cellular and Infection Microbiology · February 2024;14:1328390
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Abstract
Coagulase-negative staphylococci (CoNS) are a group of gram-positive
staphylococcal species that naturally inhabit the healthy human skin and
mucosa. The clinical impact of CoNS-associated infections has recently been
regarded as a challenge for diagnosis and therapeutic options. CoNS-associated
infections are primarily caused by bacterial resistance to antibiotics and biofilm
formation. As antibiotics are still the most used treatment, this problem will likely
persist in the future. The present study aimed to investigate the resistance and
virulence of CoNS recovered from various acne lesions and explore their genetic
basis. Skin swab samples were collected from participants with acne and healthy
skin. All samples underwent conventional culture for the isolation of CoNS,
MALDI-TOF confirmation, antibiotic susceptibility, and biofilm formation testing.
A total of 85 CoNS isolates were recovered from the samples and preliminarily
identified as Staphylococcus epidermidis. Isolates from the acne group (n = 60)
showed the highest rates of resistance to penicillin (73%), cefoxitin (63%),
clindamycin (53.3%), and erythromycin (48%), followed by levofloxacin (36.7%)
and gentamycin (31.7%). The lowest rates of resistance were observed against
tetracycline (28.3%), doxycycline (11.7%), and minocycline (8.3%). CoNS isolated
from mild, moderate acne and healthy isolates did not show strong biofilm
formation, whereas the isolates from the severe cases of the acne group showed
strong biofilm formation (76.6%). Four extensively drug-resistant and strong
biofilm-forming staphylococcal isolates recovered from patients with severe
acne were selected for whole-genome sequencing (WGS), and their genomes
were investigated using bioinformatics tools. Three of the sequenced genomes
were identified as S. epidermidis; however, isolate 29AM was identified as
Staphylococcus warneri, which is a newly emerging pathogen that is not
commonly associated with acne and was not detected by MALDI-TOF. All the
sequenced strains were multidrug-resistant and carried multiple resistance
genes, including blaZ, mecA, tet(K), erm(C), lnuA, vgaA, dfrC, fusB, fosBx1, norA,and vanT, which were found to be located on plasmids and chromosomes.
Virulence features were detected in all genomes in the presence of genes
involved in adherence and biofilm formation (icaA, icaB, icaC, sdrG, sdrH, atl,
ebh, and ebp). Only the S. warneri isolate 29AM contained immune evasion genes
(capB, capC, acpXL, and manA), an anti-phagocytosis gene (cdsA), and other
unique features. As a result of their potential pathogenicity and antibiotic
resistance, CoNS must be monitored as an emerging pathogen associated with
acne infections. To the best of our knowledge, this is the first report to isolate,
identify, and correlate S. warneri with severe acne infections among Egyptian
patients using WGS and bioinformatic analysis.
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Keywords
CoNS, acne, antibiotic resistance, virulence, genome analysis, mobilizable genetic elements, Staphylococcus epidermidis, Staphylococcus warneri