Staphylococcus aureus Interferes with Streptococci Spatial Distribution and with Protein Expression of Species within a Polymicrobial Oral Biofilm

Schnurr, Etyene; Paqué, Pune Nina; Attin, Thomas; Nanni, Paolo; Grossmann, Jonas; Holtfreter, Silva; Bröker, Barbara M.; Köhler, Christian; Diep, Binh An; Ribeiro, Apoena de Aguiar; Thurnheer, Thomas

doi:10.3390/antibiotics10020116

Cited by 10 publications

(8 citation statements)

References 88 publications

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“…According to the biofilm matrix, the mechanisms of biofilm formation can be classified as either PIA-independent or PIA-dependent ( 32 ). Previous studies found that the biofilm formation of MSSA was PIA-dependent, and the MRSA was PIA-independent ( 33 , 34 ). In contrast, all strains whether MSSA or MRSA synthesize large amounts of PIA in our study.…”

Section: Discussionmentioning

confidence: 94%

A novel small-molecule compound S-342-3 effectively inhibits the biofilm formation of Staphylococcus aureus

Zhang,

Shen,

Zhou

et al. 2023

Microbiol Spectr

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Staphylococcus aureus is an important human pathogen in both community and hospital settings that often causes persistent and recurrent infections. The continuous emergence of multidrug-resistant strains and the lag in antibiotic development make the treatment of S. aureus more challenging. The biofilm formation of S. aureus is an important reason for persistent infection. In this study, we demonstrated that a small-molecule compound S-342-3 can effectively inhibit the biofilm formation of S. aureus . The crystal violet semi-quantitative assays revealed that at a sub-minimum inhibitory concentration of 4 µg/mL, S-342-3 reduced S. aureus biofilm mass by 57.43%, 52.14%, and 25.49%. Using confocal laser scanning microscopy, we observed that the biofilm was more incompact and less uniform upon the treatment of S-342-3. At a sub-inhibitory concentration (4 µg/mL), the S-342-3 can effectively reduce the production of polysaccharide intercellular adhesin (PIA) and suppress the initial adhesion of cells in the biofilm. Consistently, the results of RT-qPCR revealed that the expression of genes associated with biofilm formation was downregulated by S-342-3 ( P < 0.05). However, we found that treatment with S-342-3 resulted in a significant decrease in the expression of global regulatory genes agrA and sarA ( P < 0.05), which play a key role in promoting cell surface attachment and PIA production in S. aureus biofilms. Also importantly, we experimentally proved that the S-342-3 was not toxic to A549 alveolar epithelial cells and the Galleria mellonella larvae. Collectively, these results suggest that the S-342-3 may be a promising anti-biofilm drug candidate with excellent biosafety, which can be further explored for its practical application in health care. IMPORTANCE Biofilms are an important virulence factor in Staphylococcus aureus and are characterized by a structured microbial community consisting of bacterial cells and a secreted extracellular polymeric matrix. Inhibition of biofilm formation is an effective measure to control S. aureus infection. Here, we have synthesized a small molecule compound S-342-3, which exhibits potent inhibition of biofilm formation in both MRSA and MSSA. Further investigations revealed that S-342-3 exerts inhibitory effects on biofilm formation by reducing the production of polysaccharide intercellular adhesin and preventing bacterial adhesion. Our study has confirmed that the inhibitory effect of S-342-3 on biofilm is achieved by downregulating the expression of genes responsible for biofilm formation. In addition, S-342-3 is non-toxic to Galleria mellonella larvae and A549 cells. Consequently, this study demonstrates the efficacy of a biologically safe compound S-342-3 in inhibiting biofilm formation in S. aureus, thereby providing a promising antibiofilm agent for further research.

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Section: Discussionmentioning

confidence: 94%

A novel small-molecule compound S-342-3 effectively inhibits the biofilm formation of Staphylococcus aureus

Zhang,

Shen,

Zhou

et al. 2023

Microbiol Spectr

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“…These species are main reservoirs of resistance genes, participating actively in the horizontal transmission of these genes to more virulent pathogens 6 , 53 , potentially including periodontal pathogens 57 . In addition, colonization of the dental biofilm by staphylococci may influence the virulence and structure of this complex oral community, triggering the change from a eubiotic biofilm to a dysbiotic one 32 – 34 , 58 . Using in vitro biofilm models, Lima et al 33 showed the ability of S. aureus to integrate and grow into a human-derived multispecies oral microbial community, affecting its composition.…”

Section: Discussionmentioning

confidence: 99%

Antimicrobial resistance and virulence of subgingival staphylococci isolated from periodontal health and diseases

Colombo

Souto

Araújo

et al. 2023

Sci Rep

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The dysbiotic biofilm of periodontitis may function as a reservoir for opportunistic human pathogens of clinical relevance. This study explored the virulence and antimicrobial susceptibility of staphylococci isolated from the subgingival biofilm of individuals with different periodontal conditions. Subgingival biofilm was obtained from 142 individuals with periodontal health, 101 with gingivitis and 302 with periodontitis, and cultivated on selective media. Isolated strains were identified by mass spectrometry. Antimicrobial susceptibility was determined by disk diffusion. The mecA and virulence genes were surveyed by PCR. Differences among groups regarding species, virulence and antimicrobial resistance were examined by Chi-square, Kruskal–Wallis or Mann–Whitney tests. The overall prevalence of subgingival staphylococci was 46%, especially in severe periodontitis (> 60%; p < 0.01). S. epidermidis (59%) and S. aureus (22%) were the predominant species across groups. S. condimenti, S. hominis, S. simulans and S. xylosus were identified only in periodontitis. High rates of resistance/reduced sensitivity were found for penicillin (60%), amoxicillin (55%) and azithromycin (37%), but multidrug resistance was observed in 12% of the isolates. Over 70% of the mecA + strains in periodontitis were isolated from severe disease. Higher detection rates of fnB + isolates were observed in periodontitis compared to health and gingivitis, whereas luxF/luxS-pvl + strains were associated with sites with deep pockets and attachment loss (p < 0.05). Penicillin-resistant staphylococci is highly prevalent in the subgingival biofilm regardless of the periodontal status. Strains carrying virulence genes related to tissue adhesion/invasion, inflammation and cytotoxicity support the pathogenic potential of these opportunists in the periodontal microenvironment.

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“…Interactions between C. albicans and Staphylococcus spp. are apparently synergistic or mutualistic, and they are increasingly reported [ 43 ]. The findings suggest that fungal cells can modulate the action of antibiotics and that bacteria can affect antifungal activity in mixed fungal–bacterial biofilms [ 44 ].…”

Section: Discussionmentioning

confidence: 99%

Analysis of Microorganism Colonization, Biofilm Production, and Antibacterial Susceptibility in Recurrent Tonsillitis and Peritonsillar Abscess Patients

Klagisa

Racenis²,

Broks³

et al. 2022

IJMS

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Background: Despite the widespread use of antibiotics to treat infected tonsils, episodes of tonsillitis tend to recur and turn into recurrent tonsillitis (RT) or are complicated by peritonsillar abscesses (PTAs). The treatment of RT and PTAs remains surgical, and tonsillectomies are still relevant. Materials and methods: In a prospective, controlled study, we analyzed the bacteria of the tonsillar crypts of 99 patients with RT and 29 patients with a PTA. We performed the biofilm formation and antibacterial susceptibility testing of strains isolated from study patients. We compared the results obtained between patient groups with the aim to identify any differences that may contribute to ongoing symptoms of RT or that may play a role in developing PTAs. Results: The greatest diversity of microorganisms was found in patients with RT. Gram-positive bacteria were predominant in both groups. Candida species were predominant in patients with a PTA (48.3% of cases). Irrespective of patient group, the most commonly isolated pathogenic bacterium was S. aureus (in 33.3% of RT cases and in 24.14% of PTA cases). The most prevalent Gram-negative bacterium was K. pneumoniae (in 10.1% of RT cases and in 13.4% of PTA cases). At least one biofilm-producing strain was found in 37.4% of RT cases and in 27.6% of PTA cases. Moderate or strong biofilm producers were detected in 16 out of 37 cases of RT and in 2 out of 8 PTA cases. There was a statistically significant association found between the presence of Gram-positive bacteria and a biofilm-formation phenotype in the RT group and PTA group (Pearson χ2 test, p < 0.001). S. aureus and K. pneumoniae strains were sensitive to commonly used antibiotics. One S. aureus isolate was identified as MRSA. Conclusions: S. aureus is the most common pathogen isolated from patients with RT, and Candida spp. are the most common pathogens isolated from patients with a PTA. S. aureus isolates are susceptible to most antibiotics. Patients with RT more commonly have biofilm-producing strains, but patients with a PTA more commonly have biofilm non-producer strains. K. pneumoniae does not play a major role in biofilm production.

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Staphylococcus aureus Interferes with Streptococci Spatial Distribution and with Protein Expression of Species within a Polymicrobial Oral Biofilm

Cited by 10 publications

References 88 publications

A novel small-molecule compound S-342-3 effectively inhibits the biofilm formation of Staphylococcus aureus

A novel small-molecule compound S-342-3 effectively inhibits the biofilm formation of Staphylococcus aureus

Antimicrobial resistance and virulence of subgingival staphylococci isolated from periodontal health and diseases

Analysis of Microorganism Colonization, Biofilm Production, and Antibacterial Susceptibility in Recurrent Tonsillitis and Peritonsillar Abscess Patients

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