Antifungal and anti-biofilm activity of a new Spanish extract of propolis against Candida glabrata

Abstract Background Resistance to traditional antifungal agents is a considerable health problem nowadays, aggravated by infectious processes related to biofilm formation, usually on implantable devices. Therefore, it is necessary to identify new antimicrobial molecules, such as natural products, to develop new therapeutic strategies to prevent and eradicate these infections. One promising product is propolis, a natural resin produced by honeybees with substances from various botanical sources, beeswax and salivary enzymes. The aim of this work was to study the effect of a new Spanish ethanolic extract of propolis (SEEP) on growth, cell surface hydrophobicity, adherence and biofilm formation of Candida glabrata, a yeast capable of achieving high levels of resistance to available anti-fungal agents. Methods The antifungal activity of SEEP was evaluated in the planktonic cells of 12 clinical isolates of C. glabrata. The minimum inhibitory concentration (MIC) of propolis was determined by quantifying visible growth inhibition by serial plate dilutions. The minimum fungicide concentration (MFC) was evaluated as the lowest concentration of propolis that produced a 95% decrease in cfu/mL, and is presented as MFC50 and MFC90, which corresponds to the minimum concentrations at which 50 and 90% of the C. glabrata isolates were inhibited, respectively. Influence on cell surface hydrophobicity (CSH) was determined by the method of microbial adhesion to hydrocarbons (MATH). The propolis effect on adhesion and biofilm formation was determined in microtiter plates by measurement of optical density (OD) and metabolic activity (XTT-assay) in the presence of sub-MIC concentrations of SEEP. Results SEEP had antifungal capacity against C. glabrata isolates, with a MIC50 of 0.2% (v/v) and an MFC50 of 0.4%, even in azole-resistant strains. SEEP did not have a clear effect on surface hydrophobicity and adhesion, but an inhibitory effect on biofilm formation was observed at subinhibitory concentrations (0.1 and 0.05%) with a significant decrease in biofilm metabolism. Conclusions The novel Spanish ethanolic extract of propolis shows antifungal activity against C. glabrata, and decreases biofilm formation. These results suggest its possible use in the control of fungal infections associated with biofilms.

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Cell surface hydrophobicity, biofilm formation, adhesives properties and molecular detection of adhesins genes in Staphylococcus aureus associated to dental caries

Microbial Pathogenesis ◽

10.1016/j.micpath.2010.03.007 ◽

2010 ◽

Vol 49 (1-2) ◽

pp. 14-22 ◽

Cited By ~ 58

Author(s):

Bochra Kouidhi ◽

Tarek Zmantar ◽

Hajer Hentati ◽

Amina Bakhrouf

Keyword(s):

Staphylococcus Aureus ◽

Dental Caries ◽

Cell Surface ◽

Biofilm Formation ◽

Molecular Detection ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity

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Quercetin inhibits virulence properties of Porphyromas gingivalis in periodontal disease

Scientific Reports ◽

10.1038/s41598-020-74977-y ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Zhiyan He ◽

Xu Zhang ◽

Zhongchen Song ◽

Lu Li ◽

Haishuang Chang ◽

...

Keyword(s):

Cell Surface ◽

Periodontal Disease ◽

Biofilm Formation ◽

Cell Structure ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Laser Scanning Microscopy ◽

Confocal Laser ◽

Antimicrobial Effects ◽

Virulence Properties

Abstract Porphyromonas gingivalis is a causative agent in the onset and progression of periodontal disease. This study aims to investigate the effects of quercetin, a natural plant product, on P. gingivalis virulence properties including gingipain, haemagglutinin and biofilm formation. Antimicrobial effects and morphological changes of quercetin on P. gingivalis were detected. The effects of quercetin on gingipains activities and hemolytic, hemagglutination activities were evaluated using chromogenic peptides and sheep erythrocytes. The biofilm biomass and metabolism with different concentrations of quercetin were assessed by the crystal violet and MTT assay. The structures and thickness of the biofilms were observed by confocal laser scanning microscopy. Bacterial cell surface properties including cell surface hydrophobicity and aggregation were also evaluated. The mRNA expression of virulence and iron/heme utilization was assessed using real time-PCR. Quercetin exhibited antimicrobial effects and damaged the cell structure. Quercetin can inhibit gingipains, hemolytic, hemagglutination activities and biofilm formation at sub-MIC concentrations. Molecular docking analysis further indicated that quercetin can interact with gingipains. The biofilm became sparser and thinner after quercetin treatment. Quercetin also modulate cell surface hydrophobicity and aggregation. Expression of the genes tested was down-regulated in the presence of quercetin. In conclusion, our study demonstrated that quercetin inhibited various virulence factors of P. gingivalis.

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Effect of Eugenol on Cell Surface Hydrophobicity, Adhesion, and Biofilm ofCandida tropicalisandCandida dubliniensisIsolated from Oral Cavity of HIV-Infected Patients

Evidence-based Complementary and Alternative Medicine ◽

10.1155/2014/505204 ◽

2014 ◽

Vol 2014 ◽

pp. 1-8 ◽

Cited By ~ 20

Author(s):

Suelen Balero de Paula ◽

Thais Fernanda Bartelli ◽

Vanessa Di Raimo ◽

Jussevania Pereira Santos ◽

Alexandre Tadachi Morey ◽

...

Keyword(s):

Cell Surface ◽

Oral Cavity ◽

Biofilm Formation ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Planktonic Cells ◽

Hydrophobic Behavior ◽

Significant Difference ◽

Substrate Surfaces ◽

Sessile Cells

MostCandidaspp. infections are associated with biofilm formation on host surfaces. Cells within these communities display a phenotype resistant to antimicrobials and host defenses, so biofilm-associated infections are difficult to treat, representing a source of reinfections. The present study evaluated the effect of eugenol on the adherence properties and biofilm formation capacity ofCandida dubliniensisandCandida tropicalisisolated from the oral cavity of HIV-infected patients. All isolates were able to form biofilms on different substrate surfaces. Eugenol showed inhibitory activity against planktonic and sessile cells ofCandidaspp. No metabolic activity in biofilm was detected after 24 h of treatment. Scanning electron microscopy demonstrated that eugenol drastically reduced the number of sessile cells on denture material surfaces. MostCandidaspecies showed hydrophobic behavior and a significant difference in cell surface hydrophobicity was observed after exposure of planktonic cells to eugenol for 1 h. Eugenol also caused a significant reduction in adhesion of mostCandidaspp. to HEp-2 cells and to polystyrene. These findings corroborate the effectiveness of eugenol againstCandidaspecies other thanC. albicans, reinforcing its potential as an antifungal applied to limit both the growth of planktonic cells and biofilm formation on different surfaces.

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Factors associated with adherence to and biofilm formation on polystyrene byStenotrophomonas maltophilia: the role of cell surface hydrophobicity and motility

FEMS Microbiology Letters ◽

10.1111/j.1574-6968.2008.01292.x ◽

2008 ◽

Vol 287 (1) ◽

pp. 41-47 ◽

Cited By ~ 94

Author(s):

Arianna Pompilio ◽

Raffaele Piccolomini ◽

Carla Picciani ◽

Domenico D'Antonio ◽

Vincenzo Savini ◽

...

Keyword(s):

Cell Surface ◽

Biofilm Formation ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Factors Associated

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Biofilm Formation and Cell Surface Properties among Pathogenic and Nonpathogenic Strains of the Bacillus cereus Group

Applied and Environmental Microbiology ◽

10.1128/aem.00155-09 ◽

2009 ◽

Vol 75 (20) ◽

pp. 6616-6618 ◽

Cited By ~ 81

Author(s):

Sandrine Auger ◽

Nalini Ramarao ◽

Christine Faille ◽

Agnès Fouet ◽

Stéphane Aymerich ◽

...

Keyword(s):

Epithelial Cells ◽

Cell Surface ◽

Bacillus Cereus ◽

Digestive Tract ◽

Biofilm Formation ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Bacillus Cereus Group ◽

Cell Surface Properties ◽

Tract Infections

ABSTRACT Biofilm formation by 102 Bacillus cereus and B. thuringiensis strains was determined. Strains isolated from soil or involved in digestive tract infections were efficient biofilm formers, whereas strains isolated from other diseases were poor biofilm formers. Cell surface hydrophobicity, the presence of an S layer, and adhesion to epithelial cells were also examined.

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Influence of freezing stress on morphological alteration and biofilm formation by Listeria monocytogenes: relationship with cell surface hydrophobicity and membrane fluidity

Archives of Microbiology ◽

10.1007/s00203-013-0921-7 ◽

2013 ◽

Vol 195 (10-11) ◽

pp. 705-715 ◽

Cited By ~ 8

Author(s):

Hanene Miladi ◽

Emna Ammar ◽

Rihab Ben Slama ◽

Nawfel Sakly ◽

Amina Bakhrouf

Keyword(s):

Listeria Monocytogenes ◽

Cell Surface ◽

Membrane Fluidity ◽

Biofilm Formation ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Freezing Stress ◽

Morphological Alteration

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Cell surface hydrophobicity and biofilm formation ability of Vibrio splendidus

Journal of Fishery Sciences of China ◽

10.3724/sp.j.1118.2011.01084 ◽

2013 ◽

Vol 18 (5) ◽

pp. 1084-1091

Author(s):

Hua LI ◽

Yang WANG ◽

Qiang LI ◽

Guo QIAO

Keyword(s):

Cell Surface ◽

Biofilm Formation ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Vibrio Splendidus

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cDNA Microarray Analysis of Differential Gene Expression in Candida albicans Biofilm Exposed to Farnesol

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.49.2.584-589.2005 ◽

2005 ◽

Vol 49 (2) ◽

pp. 584-589 ◽

Cited By ~ 164

Author(s):

Ying-Ying Cao ◽

Yong-Bing Cao ◽

Zheng Xu ◽

Kang Ying ◽

Yao Li ◽

...

Keyword(s):

Gene Expression ◽

Drug Resistance ◽

Candida Albicans ◽

Cell Surface ◽

Microarray Analysis ◽

Biofilm Formation ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Cdna Microarray Analysis ◽

Hyphal Formation

ABSTRACT Candida albicans biofilms are structured microbial communities with high levels of drug resistance. Farnesol, a quorum-sensing molecule that inhibits hyphal formation in C. albicans, has been found to prevent biofilm formation by C. albicans. There is limited information, however, about the molecular mechanism of farnesol against biofilm formation. We used cDNA microarray analysis to identify the changes in the gene expression profile of a C. albicans biofilm inhibited by farnesol. Confocal scanning laser microscopy was used to visualize and confirm normal and farnesol-inhibited biofilms. A total of 274 genes were identified as responsive, with 104 genes up-regulated and 170 genes down-regulated. Independent reverse transcription-PCR analysis was used to confirm the important changes detected by microarray analysis. In addition to hyphal formation-associated genes (e.g., TUP1, CRK1, and PDE2), a number of other genes with roles related to drug resistance (e.g., FCR1 and PDR16), cell wall maintenance (e.g., CHT2 and CHT3), and iron transport (e.g., FTR2) were responsive, as were several genes encoding heat shock proteins (e.g., HSP70, HSP90, HSP104, CaMSI3, and SSA2). Further study of these differentially regulated genes is warranted to evaluate how they may be involved in C. albicans biofilm formation. Consistent with the down-regulation of the cell surface hydrophobicity-associated gene (CSH1), the water-hydrocarbon two-phase assay showed a decrease in cell surface hydrophobicity in the farnesol-treated group compared to that in the control group. Our data provide new insight into the molecular mechanism of farnesol against C. albicans biofilm formation.

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Membrane Vesicle Formation as a Multiple-Stress Response Mechanism Enhances Pseudomonas putida DOT-T1E Cell Surface Hydrophobicity and Biofilm Formation

Applied and Environmental Microbiology ◽

10.1128/aem.01525-12 ◽

2012 ◽

Vol 78 (17) ◽

pp. 6217-6224 ◽

Cited By ~ 99

Author(s):

Thomas Baumgarten ◽

Stefanie Sperling ◽

Jana Seifert ◽

Martin von Bergen ◽

Frank Steiniger ◽

...

Keyword(s):

Stress Response ◽

Cell Surface ◽

Pseudomonas Putida ◽

Biofilm Formation ◽

Membrane Vesicle ◽

Cell Surface Hydrophobicity ◽

Surface Hydrophobicity ◽

Outer Membrane Vesicles ◽

Stress Factors ◽

Content Type

ABSTRACTAmong the adaptive responses of bacteria to rapid changes in environmental conditions, those of the cell envelope are known to be the most crucial. Therefore, several mechanisms with which bacteria change their cell surface and membranes in the presence of different environmental stresses have been elucidated. Among these mechanisms, the release of outer membrane vesicles (MV) in Gram-negative bacteria has attracted particular research interest because of its involvement in pathogenic processes, such as that ofPseudomonas aeruginosabiofilm formation in cystic fibrosis lungs. In this study, we investigated the role of MV formation as an adaptive response ofPseudomonas putidaDOT-T1E to several environmental stress factors and correlated it to the formation of biofilms. In the presence of toxic concentrations of long-chain alcohols, under osmotic stress caused by NaCl, in the presence of EDTA, and after heat shock, cells of this strain released MV within 10 min in the presence of a stressor. The MV formed showed similar size and charge properties, as well as comparable compositions of proteins and fatty acids. MV release caused a significant increase in cell surface hydrophobicity, and an enhanced tendency to form biofilms was demonstrated in this study. Therefore, the release of MV as a stress response could be put in a physiological context.

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