Propionate and Butyrate Inhibit Biofilm Formation of Salmonella Typhimurium Grown in Laboratory Media and Food Models

Abstract

Salmonella is among the most frequently isolated foodborne pathogens, and biofilm formed by Salmonella poses a potential threat to food safety. Short-chain fatty acids (SCFAs), especially propionate and butyrate, have been demonstrated to exhibit a beneficial effect on promoting intestinal health and regulating the host immune system, but their anti-biofilm property has not been well studied. This study aims to investigate the effects of propionate or butyrate on the biofilm formation and certain virulence traits of Salmonella. We investigated the effect of propionate or butyrate on the biofilm formation of Salmonella enterica serovar Typhimurium (S. Typhimurium) SL1344 grown in LB broth or food models (milk or chicken juice) by crystal violet staining methods. Biofilm formation was significantly reduced in LB broth and food models and the reduction was visualized using a scanning electron microscope (SEM). Biofilm metabolic activity was attenuated in the presence of propionate or butyrate. Meanwhile, both SCFAs decreased AI-2 quorum sensing based on reporter strain assay. Butyrate, not propionate, could effectively reduce bacterial motility. Bacterial adhesion to and invasion of Caco-2 cells were also significantly inhibited in the presence of both SCFAs. Finally, two SCFAs downregulated virulence genes related to biofilm formation and invasion through real-time polymerase chain reaction (RT-PCR). These findings demonstrate the potential application of SCFAs in the mitigation of Salmonella biofilm in food systems, but future research mimicking food environments encountered during the food chain is necessitated.

A high-sucrose diet causes microbiota composition shift and promotes the susceptibility of mice to Salmonella Typhimurium infection

“…16 Another mechanism is related to the downregulated expression of the invasion-associated gene in Salmonella Typhimurium when exposed to SCFAs. 15,36,37 Meanwhile, the levels of Bacteroidetes over Firmicutes were higher in the control diet mice, which has been reported to be associated with decreased susceptibility to the burdens of C. rodentium. 38 We also found that the abundance of Proteobacteria improved in HSD mice after infection, which has previously been reported to be associated with intestinal epithelial dysfunction.…”

Gut microbiome derived short chain fatty acids: Promising strategies in necrotising enterocolitis

“…However, more recent research reported an increase of acetic acid related to the colonisation of the specific strain Bifidobacterium breve BBG-001 in preterm neonates, but with no statistically significant difference on intestinal barrier function ( Fleming et al., 2021 ). More recent studies, such as the one performed by Liu et al. (2022) , indicated a decrease of Bifidobacterium subs.…”

“…SCFAs have been used in the agricultural industry because of their intrinsic broad-spectrum antimicrobial effect. Important examples in food production and human studies include the addition of butyric acid to control Salmonella ( Liu et al. 2022 ) and the ability of SCFAs to reduce the growth and virulence of pathogenic E. coli in a pH dependant manor ( Zhang et al., 2020 ).…”

“… Modified gas chromatography–mass spectrometry Huang et al., 2022 Ex vivo In vitro Fetal mouse jejunum cultures Human fetal intestinal epithelial FHs 74 Int cells The addition of SCFAs (Acetic, butyric and propionic acid) decreased the inflammatory response induced by IL-1B through inhibiting ERK1/2 pathway; NF-κB p65, JNK1/2, and ERK1/2 pathways, or NF-κB p65 and ERK1/2 pathways. Liu et al. 2022 In vivo (Human model) Preterm infants <34 weeks: n = 34 NEC: n = 17 Control: n = 17 SCFAs (acetic acid, propanoic acid, and butyric acid) were significantly lower in the NEC group both before and at the moment of diagnosis ( p < 0.05).…”

Effects of Salmonella Typhimurium Infection on the Gut Microbiota of Cherry Valley Meat Ducks

“…Many studies have shown that butyric acid, one of the short-chain fatty acids, has the effect of inhibiting Salmonella [ 22 , 23 , 24 ]. Ruminococcaceae [ 25 , 26 ] and Lachnospiraceae [ 27 ] are important producers of butyric acid in the intestine. Studies have reported that the abundance of Ruminococcaceae and Lachnospiraceae in the intestinal tract of chicks infected with Salmonella is inversely proportional to the abundance of Enterobacteriaceae [ 18 ].…”