Abstract
Salmonella spp. may form biofilm, and bacteria in biofilm are more resistant to drug, chemical, physical and mechanical stresses, and host immune system. The progress on biofilm research will be helpful for the development of new tools and strategies to prevent biofilm-related disease and decontaminate biofilm-derived Salmonella in food production. In this review, we present a comprehensive overview of biofilm formation in Salmonella, included that (1) the component of Salmonella biofilm, (2) the detection methods for biofilm, (3) the identification of biofilm-formation-associated genes, (4) the regulation mechanism of biofilm formation, and (5) virulence or resistance of Salmonella in biofilm.
Keywords
- Salmonella
- biofilm
- component
- mechanism
- gene
- pathogenicity
- drug resistance
1. Introduction
2. The component of Salmonella biofilm
The biofilm formation is a multistep developmental process that always has several distinguishable steps: (a) attachment to the carrier surface, reversible, (b) irreversible attachment, binding to the surface with the participation of adhesions or exopolysaccharides, (c) the development of microcolonies, a distinct mushroom shape, (d) the maturation of biofilm architecture [11, 12], (e) under favorable conditions, the synthesis of martrix compounds decreases and the matrix is enzymatically cleaved, leading to biofilm dispersion [13]. In natural environments,
The extracellular matrix of
3. The detection methods for biofilm
3.1. Quantification of biofilm formation
Biofilm formation of
3.2. Biofilm formation in glass tube
The overnight cultures of bacteria are diluted 1:100 in the diluted TSB. Two milliliters of each bacterial suspension are added into borosilicate glass tubes and incubated at 28°C for 48 h. Then, the liquid is decanted and the tubes are washed gently three times with distilled water. Two ml of 0.4% crystal violet (v/v) are added into each tube and stained at room temperature for 20 min. The stained biofilm is observed at the liquid–air interface on the glass test tube walls or at the bottom of the tube [46]. The glass tubes may also be incubated at 37°C at 200 rpm by using an orbital shaker, and biofilm is observed at interphase without staining [47].
3.3. Congo red/carbol fuchsin staining
The overnight culture (1:100 diluted in TSB) is inoculated into 3 ml of fresh TSB in a 6-well plate containing sterile polystyrene coverslip (20 × 20 mm). After incubation at 28°C for 24 or 48 h without agitation, the coverslips are removed carefully, treated with cetylpyridinium chloride (10 mM) for 30 s, rinsed with distilled water and air dried for 20–30 min. After fixation by gentle heating, the coverslips are stained with a mixture of saturated aqueous Congo red solution and 10% Tween-80 (2:1, V/V) for 30 min and rinsed with distilled water. After staining with 10% (v/v) Ziehl carbol fuchsin for 6 min and rinsing in distilled water, the coverslips are air dried and mounted on slides [48]. Under a light microscope, bacterial cells on slides show purple staining, while the exopolysaccharides of biofilm show pink staining [46].
3.4. Field emission scanning electron microscopy
The coverslips with cultured bacteria are fixed in 3% glutaraldehyde in 0.1 M phosphate-buffered saline at 4°C for 2 h. The samples are then dehydrated with increasing concentrations of ethanol (50, 70, 80, 90, and 100%) followed by isoamyl acetate (100%), each for 15 min. The samples are critical point dried for 5 h, coated with gold palladium alloy, and observed under a field emission scanning electron microscope [49]. The biofilm-formation strain exhibits increased clusters of bacteria cells with curli fimbriae and has meshwork-like structures surrounding the cell surfaces.
3.5. Congo red and calcofluor plates
LB agar plate without salt supplemented with 40 mg/L Congo red and 20 mg/L brilliant blue is used to determine the Congo red-binding property of the colonies. LB agar plate supplemented with 200 mg/L calcofluor (fluorescent brightener) is used to determine the cellulose production by comparing the fluorescence of the test strains under UV light [49]. Biofilm of
3.6. Confocal laser microscopy
Bacteria cultured on coverslipes, dish, or microplate are stained by 0.1 M phosphate-buffered saline (pH 7.2) containing SYTO 9 and propidium iodide. After 10 min incubation in the dark at room temperature, stained samples are examined using a confocal scanning laser microscopy. Fluorochromes are excited using an argon laser source at 488 nm. Images are collected in two channels, 490–515 and 620–640 nm, corresponding to the emission maxima for SYTO 9 and propidium iodide, respectively. Optical sections approximately 1 μm in height are collected starting from below the focal plane to upward through the entire biofilm. The biofilm cells are clearly observed in a multilayer community [20, 51].
4. Identification of biofilm-formation–associated genes
The most common biofilm-formation–associated genes are the genes encode adhesins. The best characterized of the
Pathogenicity islands accommodate large clusters of genes that contribute to a particular virulence phenotype.
Lipopolysaccharide (LPS) synthesis also involves the biofilm formation of
5. Regulation mechanism of biofilm formation
Biofilm formation is majorly regulated by CsgD protein, a regulator belonging to the LuxR family [69]. CsgD has an N-terminal receiver domain with a conserved aspartate (D59) as a putative target site for phosphorylation and a C-terminal LuxR-like helix-turn-helix DNA binding motif. The unphosphorylated CsgD directly binds the
c-di-GMP is recognized as a ubiquitous bacterial second messenger and a key regulator in bacterial transition from a motile and planktonic to a sessile and biofilm lifestyle. High intracellular c-di-GMP levels promote extracellular matrix production and subsequent biofilm formation and repress motility, whereas low intracellular c-di-GMP levels suppress matrix production and promote single-cell motility [77]. The synthesis/degradation of c-di-GMP depends on diguanylate cyclase/phosphodiesterase enzymatic activities. The cyclase activity, which converts two molecules of GTP to c-di-GMP, is encoded in the GGDEF protein domain, while phosphodiesterase activity, which hydrolyzes c-di-GMP to linear 5′-pGpG or two GMP molecules, is encoded in the EAL and HD-GYP domains. For example, Adar, containing a GGDEF domain, encodes diguanylate cyclase synthesizing c-di-GMP, is required for cellulose production and biofilm formation. In another seven GGDEF family (GcpA-G), only GcpA and GcpE are critical for biofilm formation [37]. The EAL domain protein STM4264, STM3611, and the GGDEF-EAL domain protein STM1703 play a determinative role in the expression level of multicellular behavior of
CsgD synthesis is also regulated at the post-transcriptional level by sRNA. sRNAs have emerged as a diverse group of trans- or cis-encoded regulatory molecules of approximately 50–250 nt in size. The RNA chaperone Hfq protects sRNAs form degradation and facilitates their binding to the target mRNAs. All these sRNA may negatively regulate
Many gram-negative bacteria utilize N-acyl-L-homoserine lactones (AHLs) to bind to transcriptional regulators leading to activation or repression of target genes.
6. Virulence or resistance for biofilm
Biofilm formation may involve in the virulence of
The
The
BapA, a large cell-surface protein, is required for biofilm formation by
Besides, the constitutional components of biofilm, there are many regulation proteins involved in both biofilm formation and virulence. An
In summary,
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