Salmonella enterica induces biogeography-specific changes in the gut microbiome of pigs

Authors: GOMES-NETO, JOAO CARLOS - University Of Nebraska; PAVLOVIKJ, NATASHA - University Of Nebraska; KORTH, NATE - University Of Nebraska; NABERHAUS, SAMANTHA - Iowa State University; Arruda, Bailey; BENSON, ANDREW - University Of Nebraska; KREUDER, AMANDA - Iowa State University

Submitted to: Frontiers in Veterinary Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/18/2023
Publication Date: 9/14/2023
Citation: Gomes-Neto, J., Pavlovikj, N., Korth, N., Naberhaus, S.A., Arruda, B.L., Benson, A.K., Kreuder, A.J. 2023. Salmonella enterica induces biogeography-specific changes in the gut microbiome of pigs. Frontiers in Veterinary Science. https://doi.org/10.3389/fvets.2023.1186554.
DOI: https://doi.org/10.3389/fvets.2023.1186554

Interpretive Summary: Swine are a major reservoir of an array of zoonotic Salmonella enterica subsp including Derby, Monophasic (4,[5],12:i:-), and Typhimurium. Despite numerous investigations and methodologies aimed at decreasing the carriage of Salmonella, swine continues to be a major source of human exposure to S. enterica. In this study, we assessed the gastrointestinal (GI) microbiome composition of pigs in different intestinal compartments following infection with specific zoonotic serovars of S. enterica. Apart from the control (sham-inoculated) animals (n = 12), 20 nursery pigs were infected with one of the following serovars: S. Derby, S. Monophasic, and S. Typhimurium. 16S metagenomics was then performed to assess for GI microbiome changes in terms of diversity and specific taxa alterations across several GI biogeographies (small and large intestine, feces) and days post-infection (DPI) 2, 4, and 28; these results were then compared to the amount of inflammation present in the tissue. Only S. Typhimurium could induce significant diversity changes. However, at the taxonomic level, Prevotella 9 was found to be significantly reduced in all Salmonella infected groups compared to the control group at DPI 4 in the colonic apex. Additionally, three putative short-chain fatty acid producing taxa were on average negatively correlated with tissue inflammation. Prevotella 9 was also found in lower proportion in colonic apex samples from S. Typhimurium-infected animals that presumably had chronic large intestinal inflammation as compared to those without signs of chronic inflammation. In conclusion, this work further elucidates that distinct swine-related zoonotic serovars of S. enterica can induce both shared and unique alterations in gut microbiome biogeography, which helps inform future investigations of dietary modifications aimed at increasing colonization resistance against Salmonella through GI microbiome alterations.

Technical Abstract: Swine are a major reservoir of an array of zoonotic Salmonella enterica subsp. Enterica lineage I serovars including Derby, Monophasic (4,[5],12:i:-), and Typhimurium. Despite numerous investigations and methodologies aimed at decreasing the carriage of Salmonella, swine continues to be a major source of human exposure to S. enterica, including multi-drug resistant serovar-specific lineages. In this study, we assessed the gastrointestinal (GI) microbiome composition of pigs in different intestinal compartments following infection with specific zoonotic serovars of S. enterica. Apart from the control (sham-inoculated) animals (n = 12), 20 nursery pigs were infected with one of the following serovars: S. Derby, S. Monophasic, and S. Typhimurium. 16S metagenomics was then performed to assess for GI microbiome changes in terms of diversity (alpha and beta) and specific taxa alterations across several GI biogeographies (small and large intestine, feces) and days post-infection (DPI) 2, 4, and 28; these results were then compared to disease phenotypes including histopathology. In terms of GI microbiome diversity, only S. Typhimurium could induce significant changes at the alpha- (Simpson’s and Shannon’s indexes) and beta-diversity levels, specifically at the peak of inflammation (DPI 4) and only in the colonic apex. However, at the taxonomic level, Prevotella 9 was found to be significantly reduced in all Salmonella infected groups compared to the control at DPI 4 in the colonic apex. Additionally, three putative short-chain fatty acid producing taxa (Prevotella 9, Faecalibacterium, and Clostridium sensu stricto 1) were on average negatively correlated with histopathology scores. Prevotella 9 was also found in lower proportion in colonic apex samples from S. Typhimurium-infected animals that presumably had chronic large intestinal inflammation as compared to those without signs of chronic inflammation. In conclusion, this work further elucidates that distinct swine-related zoonotic serovars of S. enterica can induce both shared and unique alterations in gut microbiome biogeography, which helps inform future investigations of dietary modifications aimed at increasing colonization resistance against Salmonella through GI microbiome alterations.