Inhibition of Salmonella binding to porcine intestinal cells by a wood-derived prebiotic

Authors: BOŽIC, ALEKSANDAR - University Of Novi Sad; Anderson, Robin; Crippen, Tawni - Tc; Swaggerty, Christina - Christi; Hume, Michael; Beier, Ross; He, Louis; Genovese, Kenneth - Ken; Poole, Toni; Harvey, Roger; Nisbet, David

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/14/2020
Publication Date: 7/15/2020
Publication URL: https://handle.nal.usda.gov/10113/7057976
Citation: Božic, A., Anderson, R.C., Crippen, T.L., Swaggerty, C.L., Hume, M.E., Beier, R.C., He, L.H., Genovese, K.J., Poole, T.L., Harvey, R.B., Nisbet, D.J. 2020. Inhibition of Salmonella binding to porcine intestinal cells by a wood-derived prebiotic. Microorganisms. 8(7):1051. https://doi.org/10.3390/microorganisms8071051.
DOI: https://doi.org/10.3390/microorganisms8071051

Interpretive Summary: Salmonella is a foodborne pathogen that can cause contamination of animal-produced foods. Additionally, antimicrobial resistance in Salmonella may render antibiotics ineffective and provides motivation to develop non-antibiotic strategies to control animal diseases. Prebiotic products capable of blocking pathogen adherence to the animal’s intestinal mucosa are attractive alternatives to antibiotics as these have potential to prevent enteric infections. Presently, a wood-derived prebiotic was found to inhibit binding of Salmonella and pathogenic Escherichia coli strains to a yeast strain commonly used to test binding affinities. Tests for the ability of the prebiotic to prevent binding of Salmonella to intestinal cells obtained from a pig revealed that the prebiotic treatment prevented binding of the Salmonella to 32 to 34% fewer individual IPEC-J2 cells when compared to binding by Salmonella not treated with the prebiotic. Quantitatively, 90% fewer prebiotic-treated Salmonella cells were bound per individual intestinal cell compared to counts obtained for non-prebiotic treated Salmonella. Comparison of the ability of the Salmonella to invade into the inside of the intestinal cells revealed greater than 90% decrease in intracellular recovery of prebiotic-treated Salmonella compared to non-treated Salmonella (averaging 4.4 ± 0.2 Log10 CFU/well). These results demonstrate that compounds within the wood-derived prebiotic bind surface sites normally used by Salmonella to attach and invade into intestinal cells. These findings may ultimately be used in development of natural treatment to prevent Salmonella infections in food-producing animals. This research will help farmers produce wholesome, microbiological safe food at less cost for the American consumer.

Technical Abstract: Numerous Salmonella enterica serovars can cause disease and contamination of animal-produced foods. Antimicrobial resistance in these as well as other bacteria in animal agriculture may render antibiotics ineffective and provides motivation to develop non-antibiotic strategies to control animal diseases. Oligosaccharide-rich products capable of blocking pathogen adherence to the animal’s intestinal mucosa are attractive alternatives to antibiotics as these have potential to prevent enteric infections. Presently, a wood-derived prebiotic composed mainly of glucose-galactose-mannose-xylose oligomers was found to inhibit mannose-sensitive binding of select Salmonella enterica serovar Typhimurium and enteropathogenic Escherichia coli strains when reacted with Saccharomyces boulardii. Tests for the ability of the prebiotic to prevent binding of a green fluorescent protein (GFP)-labeled Salmonella Typhimurium to intestinal porcine epithelial cells (IPEC-J2) cultured in vitro revealed that prebiotic-exposed GFP-labeled S. Typhimurium suspensions bound 32 to 34% fewer (P < 0.05) individual IPEC-J2 cells than did GFP-labeled S. Typhimurium suspensions having no prebiotic exposure. Quantitatively, 90% fewer (P < 0.05) prebiotic-exposed GFP-labeled S. Typhimurium cells were bound per individual IPEC-J2 cell compared to counts obtained for non-prebiotic exposed GFP-labeled S. Typhimurium, the latter, depending on challenge level, averaging 0.26 to 13.77 GFP-labeled S. Typhimurium cells/IPEC-J2 cell, respectively. Comparison of invasiveness of S. Typhimurium DT104 against IPEC-J2 cells revealed greater than 90% decrease (P < 0.05) in intracellular recovery of prebiotic-exposed S. Typhimurium DT104 when compared to non-exposed controls (averaging 4.4 ± 0.2 Log10 CFU/well). These results suggest compounds within the wood-derived prebiotic bound to E. coli- and S. Typhimurium-produced adhesions and in the case of S. Typhimurium, this adhesion-binding activity inhibited the binding and invasion of IPEC-J2 cells.