Abstract
Salmonella biofilms act as a continuous source for cross-contamination in the food processing environments. In this study, a stable rugose morphotype of Salmonella was first induced by sequential exposure to subinhibitory concentrations (SICs) of sodium hypochlorite (NaOCl) (ranging from 50 to 300 ppm over 18-day period) in tryptic soy broth. Then, rugose and smooth morphotypes of Salmonella Typhimurium ATCC 14028 and Salmonella Heidelberg ATCC 8326 were characterized for biofilm forming abilities on polystyrene and stainless steel surfaces. Rugose morphotype of both ATCC 14028 and ATCC 8326 exhibited higher Exopolysaccharide (EPS) formation than smooth morphotype (p ≤ 0.05). Also, the SICs of NaOCl (200 or 300 ppm in broth model) increased the biofilm formation ability of rugose morphotype of ATCC 8326 (p ≤ 0.05) but decreased that of ATCC 14028. The 2-day-old Salmonella biofilms were treated with biocidal concentrations of 50, 100, or 200 ppm NaOCl (pH 6.15) in water for 5, 10, or 20 min at room temperature. The biofilm reduction in CFU/cm2 for the rugose was lower than the smooth morphotype on both surfaces (p ≤ 0.05) by lethal NaOCl in water. Scanning electron micrographs on both polystyrene and stainless steel surfaces demonstrated that the rugose morphotype produced a denser biofilm than the smooth morphotype. Transmission electron micrographs revealed the cell wall roughness in rugose morphotype, which may help in tolerance to NaOCl. The gene expression data indicate that the expression of biofilm regulator (csgD), curli (csgA, csgB, and csgC), and cellulose (bcsE) was significantly increased in rugose morphotype when induced by sequential exposure of NaOCl SICs. These findings reveal that the rugose morphotype of S. Typhimurium and S. Heidelberg produced significantly denser biofilm on food contact surfaces, which also increased with sequential exposure to SICs of NaOCl in the case of S. Heidelberg, and these biofilms were more tolerant to biocidal NaOCl concentrations commonly used in the food processing plants.
Highlights
Every year, foodborne salmonellosis caused by non-typhoidal Salmonella is responsible for 380 deaths and 19,000 hospitalizations in the USA (Scallan et al, 2011)
Salmonella cell aggregates and pellicle formation were observed after daily passages for 18 days in the presence of subinhibitory NaOCl in tryptic soy broth (TSB) at 37°C
An aliquot of overnight incubated rugose culture in TSB was plated on tryptic soy agar (TSA) and characteristic corrugated and dry morphology was formed after 24 h at 37°C
Summary
Foodborne salmonellosis caused by non-typhoidal Salmonella is responsible for 380 deaths and 19,000 hospitalizations in the USA (Scallan et al, 2011). Often Salmonella forms biofilms on different food contact surfaces (Stepanovic et al, 2004). In the food processing facilities, disinfectants such as sodium hypochlorite (NaOCl), quaternary ammonium compounds (QAC), and organic acids such as peroxyacetic acid and acetic acid are frequently used (Russell and McDonnell, 2000). Previous findings show that the gradual exposure to sublethal concentration of antimicrobials (including disinfectants) induces bacterial adaptation that leads to the development of antimicrobial tolerant phenotypes of foodborne bacterial pathogens (Abeysundara et al, 2016; Bansal et al, 2018)
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