Effects of environmental conditions (temperature, pH, and glucose) on biofilm formation of Salmonella enterica serotype Kentucky and virulence gene expression

Abstract

Salmonella is a foodborne pathogen and an emerging zoonotic bacterial threat in the food industry. The aim of this study was to evaluate the biofilm formation by a cocktail culture of 3 wild isolates of Salmonella enterica serotype Kentucky on plastic ( PLA ), silicon rubber ( SR ), and chicken skin surfaces under various temperatures (4, 10, 25, 37, and 42°C) and pH values (4.0, 5.0, 6.0, 7.0, and 8.0). Then, at the optimum temperature and pH, the effects of supplementation with glucose (0, 0.025, 0.05, and 0.4% w/v) on biofilm formation were assessed on each of the surfaces. The results indicated that higher temperatures (25 to 42°C) and pH values (7.0 and 8.0) led to more robust biofilm formation than lower temperatures (4 and 10°C) and lower pH levels (4.0 to 6.0). Moreover, biofilm formation was induced by 0.025% glucose during incubation at the optimum temperature (37°C) and pH (7.0) but inhibited by 0.4% glucose. Consistent with this finding, virulence related gene ( rpoS, rpoH, hilA , and avrA ) expression was increased at 0.025% glucose and significantly reduced at 0.4% glucose. This results also confirmed by field emission scanning electron microscope, confocal laser scanning microscopy, and autoinducer-2 determination. This study concluded that optimum environmental conditions (temperature 37°C, pH 7.0, and 0.25% glucose) exhibited strong biofilm formation on food and food contract surfaces as well as increased the virulence gene expression levels, indicating that these environmental conditions might be threating conditions for food safety.

Impact of Quercetin against Salmonella Typhimurium Biofilm Formation on Food–Contact Surfaces and Molecular Mechanism Pattern

“…The incidence of salmonellosis has grown because of the presence of salmonella spp. biofilm on numerous food-contact surfaces in poultry and chicken processing plants [ 4 ].…”

“…Biofilm is a bacterial structure population that is permanently adherent to biotic and abiotic surfaces and incorporated in a self-produced extracellular polymeric matrix [ 5 , 6 ]. Biofilm production on foods and food-contact surfaces results in contamination, post-process contamination, and cross-contamination of the final product, resulting in food spoiling, product rejection, economic losses, and foodborne diseases [ 4 , 7 , 8 ]. Bacteria in biofilms are more adaptable to varied environmental conditions than planktonic cells.…”

“…RpoS is a stress response protein that regulates the expression of genes linked to resistance to various environmental challenges (such as hunger, oxidative damage, and low pH), and environmental stress is linked to biofilm formation [ 12 ]. AvrA and hilA are virulence genes associated with invasiveness in Salmonella pathogenicity islands-1 (SPI-1) [ 4 ]. LuxS is associated with the quorum-sensing through the synthesis of AI-2 (autoinducer-2) molecules [ 8 , 13 ].…”

Genetic Characterization of Salmonella Infantis with Multiple Drug Resistance Profiles Isolated from a Poultry-Farm in Chile

“…However, the constant use of these chemical solutions triggers tolerance, adaptation, and resistance to these agents [35,36]. Therefore, the continuous sanitization of production lines might actually enhance bacterial pathogenicity and should therefore be a major concern for the food industry and health officials, especially considering the current scenario of shifted serovar prevalence and emergence of MDR strains [37][38][39]. In this context, from 2014 to 2018, the number of clinical cases associated with S. Infantis strains incremented in Chile [40], and were usually associated with MDR.…”

Persistence of Salmonella enterica and Enterococcus faecium NRRL B-2354 on Baby Spinach Subjected to Temperature Abuse after Exposure to Sub-Lethal Stresses

“…Our findings demonstrate that S. enterica , previously adaptive to desiccation, took greater advantage of the favorable condition at the abusive temperature to resuscitate and persist on baby spinach. One conceivable explanation could be that the biosynthesis of curli in S. enterica was inhibited during the cold storage at 4 °C while dramatically increased at the abusive temperature at 37 °C [ 38 , 39 ]. The contamination of leafy greens by desiccation-stressed cells can be a major concern for the food industry due to their extended persistence after being subjected to temperature abuse.…”