Low concentrations of ethanol stimulate biofilm and pellicle formation in <i>Pseudomonas aeruginosa</i>

Tashiro, Yosuke; Inagaki, Aya; Ono, Kaori; Inaba, Tomohiro; Yawata, Yutaka; Uchiyama, Hiroo; Nomura, Nobuhiko

doi:10.1080/09168451.2014.877828

Cited by 39 publications

(31 citation statements)

References 24 publications

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“…The maximum biofilm formation was observed for 2.5% ethanol for moderate and 1.25% ethanol for weak biofilm forming isolates. This finding is in agreement with previous studies [36] where elevated biofilm formation was observed after application of 1-2% ethanol. Ethanol, at 2.4% v/v, enhanced the expression of a number of biofilm-promoting genes in S. aureus [38].…”

Section: Discussionsupporting

confidence: 94%

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Changes in the Expression of Biofilm-Associated Surface Proteins inStaphylococcus aureusFood-Environmental Isolates Subjected to Sublethal Concentrations of Disinfectants

Cincarova

Polanský

Babák

et al. 2016

BioMed Research International

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Sublethal concentrations (sub-MICs) of certain disinfectants are no longer effective in removing biofilms from abiotic surfaces and can even promote the formation of biofilms. Bacterial cells can probably adapt to these low concentrations of disinfectants and defend themselves by way of biofilm formation. In this paper, we report on three Staphylococcus aureus biofilm formers (strong B+++, moderate B++, and weak B+) that were cultivated with sub-MICs of commonly used disinfectants, ethanol or chloramine T, and quantified using Syto9 green fluorogenic nucleic acid stain. We demonstrate that 1.25–2.5% ethanol and 2500 μg/mL chloramine T significantly enhanced S. aureus biofilm formation. To visualize differences in biofilm compactness between S. aureus biofilms in control medium, 1.25% ethanol, or 2500 μg/mL chloramine T, scanning electron microscopy was used. To describe changes in abundance of surface-exposed proteins in ethanol- or chloramine T-treated biofilms, surface proteins were prepared using a novel trypsin shaving approach and quantified after dimethyl labeling by LC-LTQ/Orbitrap MS. Our data show that some proteins with adhesive functions and others with cell maintenance functions and virulence factor EsxA were significantly upregulated by both treatments. In contrast, immunoglobulin-binding protein A was significantly downregulated for both disinfectants. Significant differences were observed in the effect of the two disinfectants on the expression of surface proteins including some adhesins, foldase protein PrsA, and two virulence factors.

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Section: Discussionsupporting

confidence: 94%

“…Tolerance of bacterial biofilms to disinfectants increases the risk of cross-contamination of food. Bacterial cells probably react to the presence of disinfectants and defend themselves by way of biofilm formation [36]. As disinfectants diffuse through the biofilm matrix their concentration is lowered and bacterial cells can adapt.…”

Section: Discussionmentioning

confidence: 99%

Changes in the Expression of Biofilm-Associated Surface Proteins inStaphylococcus aureusFood-Environmental Isolates Subjected to Sublethal Concentrations of Disinfectants

Cincarova

Polanský

Babák

et al. 2016

BioMed Research International

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“…After the planktonic cells were removed, crystal violet staining and the quantification of biofilms were performed as previously described (3). The biofilm was visualized using confocal laser scanning microscopy (CLSM) as previously described (33). The cells were grown in Nunc flasks, and the attached biofilm was observed using a Carl Zeiss Pascal laser scanning microscope equipped with a 63ϫ/1.4-numerical aperture Plan-Apochromat objective and a 40ϫ/0.80-numerical aperture IR Achroplan W water immersion objective (Carl Zeiss, Jena, Germany).…”

Section: Methodsmentioning

confidence: 99%

Inhibition of Pseudomonas aeruginosa Swarming Motility by 1-Naphthol and Other Bicyclic Compounds Bearing Hydroxyl Groups

Oura

Tashiro

Toyofuku

et al. 2015

Appl Environ Microbiol

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cMany bacteria convert bicyclic compounds, such as indole and naphthalene, to oxidized compounds, including hydroxyindoles and naphthols. Pseudomonas aeruginosa, a ubiquitous bacterium that inhabits diverse environments, shows pathogenicity against animals, plants, and other microorganisms, and increasing evidence has shown that several bicyclic compounds alter the virulence-related phenotypes of P. aeruginosa. Here, we revealed that hydroxyindoles (4-and 5-hydroxyindoles) and naphthalene derivatives bearing hydroxyl groups specifically inhibit swarming motility but have minor effects on other motilities, including swimming and twitching, in P. aeruginosa. Further analyses using 1-naphthol showed that this effect is also associated with clinically isolated hyperswarming P. aeruginosa cells. Swarming motility is associated with the dispersion of cells from biofilms, and the addition of 1-naphthol maintained biofilm biomass without cell dispersion. We showed that this 1-naphthol-dependent swarming inhibition is independent of changes of rhamnolipid production and the intracellular level of signaling molecule cyclic-di-GMP (c-di-GMP). Transcriptome analyses revealed that 1-naphthol increases gene expression associated with multidrug efflux and represses gene expression associated with aerotaxis and with pyochelin, flagellar, and pilus synthesis. In the present study, we showed that several bicyclic compounds bearing hydroxyl groups inhibit the swarming motility of P. aeruginosa, and these results provide new insight into the chemical structures that inhibit the specific phenotypes of P. aeruginosa.

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“…This may be due to enhanced production of cytotoxic phospholipase C and increased expression of nutrient uptake pathways (18). In P. aeruginosa , ethanol produced by C. albicans influences the expression of the antifungal phenazine 5-methyl phenazine-1-carboxylic acid (5MPCA) and 1% ethanol was sufficient to modulate phenazine production and stimulate the exopolysaccharide Pel and Psl-mediated biofilm and pellicle formation (13, 16).…”

Section: Introductionmentioning

confidence: 99%

Ethanol stimulates trehalose production through a SpoT-DksA-AlgU dependent pathway inPseudomonas aeruginosa

Harty

Martins

Doing

et al. 2019

Preprint

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24Pseudomonas aeruginosa frequently resides among ethanol-producing microbes, 25 making its response to these microbially-produced concentrations of ethanol relevant to 26 understanding its biology. Our ranscriptome analysis found that the genes involved in 27 trehalose metabolism were induced by low concentrations of ethanol, and levels of intracellular 28 trehalose increased significantly upon growth with ethanol. The increase in trehalose was 29 dependent on the TreYZ pathway, but not other trehalose metabolic enzymes TreS or TreA. 30The sigma factor AlgU (AlgT), a homolog of RpoE in other species, was required for increased 31 expression of the treZ gene and trehalose levels, but induction was not controlled by the well-32 characterized proteolysis of its antisigma factor MucA. Growth with ethanol led to increased 33SpoT-dependent (p)ppGpp accumulation, which stimulates AlgU-dependent transcription of 34 treZ and other AlgU-regulated genes through DksA, a (p)ppGpp and RNA polymerase binding 35 protein. Ethanol stimulation of trehalose also required acylhomoserine lactone (AHL)-mediated 36 quorum sensing, as induction was not observed in a ∆lasR∆rhlR strain. A network analysis 37 using a model, eADAGE, built from publicly available P. aeruginosa transcriptome datasets (1) 38 provided strong support for our model that treZ and co-regulated genes are controlled by both 39AlgU and AHL-mediated QS (QS). Consistent with (p)ppGpp and AHL-mediated quorum 40 sensing regulation, ethanol, even when added at the time of culture inoculation, stimulated treZ 41 transcript levels and trehalose production in cells from post-exponential phase cultures but not 42 from exponential phase cultures. These data highlight the integration of growth and cell density 43 cues in the P. aeruginosa transcriptional response to ethanol. 44 Importance 45Pseudomonas aeruginosa is often found with bacteria and fungi that produce 46 fermentation products including ethanol. At concentrations similar to those produced by 47 environmental microbes, we found that ethanol stimulated expression of trehalose biosynthetic 48 genes and cellular levels of trehalose, a disaccharide that protects against environmental 49 stresses. The induction of trehalose by ethanol required the alternative sigma factor AlgU 50 through DksA and SpoT-dependent (p)ppGpp. Trehalose accumulation also required AHL 51 quorum sensing and only occurred in post-exponential phase cultures. This work highlights 52 how cells integrate cell-density and growth cues in their responses to products made by other 53 microbes and a reveals a new role for (p)ppGpp in the regulation of AlgU activity. 55Pseudomonas aeruginosa is a ubiquitous Gram-negative bacterium that can cause 56 acute and chronic infections in a broad range of hosts. P. aeruginosa frequently causes 57 chronic infections in individuals with the genetic disorder cystic fibrosis (CF). Diverse bacterial 58 and fungal taxa often co-infect with P. aeruginosa in CF airways (2-6), and many of these taxa 59 are robust fermenters c...

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Low concentrations of ethanol stimulate biofilm and pellicle formation in Pseudomonas aeruginosa

Cited by 39 publications

References 24 publications

Changes in the Expression of Biofilm-Associated Surface Proteins inStaphylococcus aureusFood-Environmental Isolates Subjected to Sublethal Concentrations of Disinfectants

Changes in the Expression of Biofilm-Associated Surface Proteins inStaphylococcus aureusFood-Environmental Isolates Subjected to Sublethal Concentrations of Disinfectants

Inhibition of Pseudomonas aeruginosa Swarming Motility by 1-Naphthol and Other Bicyclic Compounds Bearing Hydroxyl Groups

Ethanol stimulates trehalose production through a SpoT-DksA-AlgU dependent pathway inPseudomonas aeruginosa

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