Influence of the intestinal microbiota on colonization resistance to Salmonella and the shedding pattern of naturally exposed pigs

Argüello, Héctor and Estellé, Jordi and Leonard, Finola C. and Crispie, Fiona and Cotter, Paul D. and O’Sullivan, Orla and Lynch, Helen and Walia, Kavita and Duffy, Geraldine and Lawlor, Peadar G. and Gardiner, Gillian E. (2019) Influence of the intestinal microbiota on colonization resistance to Salmonella and the shedding pattern of naturally exposed pigs. mSystems, 4 (2). ISSN 2379-5077

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Abstract

Salmonella colonization and infection in production animals such as pigs are a cause for concern from a public health perspective. Variations in susceptibility to natural infection may be influenced by the intestinal microbiota. Using 16S rRNA compositional sequencing, we characterized the fecal microbiome of 15 weaned pigs naturally infected with Salmonella at 18, 33, and 45 days postweaning. Dissimilarities in microbiota composition were analyzed in relation to Salmonella infection status (infected, not infected), serological status, and shedding pattern (nonshedders, single-point shedders, intermittent-persistent shedders). Global microbiota composition was associated with the infection outcome based on serological analysis. Greater richness within the microbiota postweaning was linked to pigs being seronegative at the end of the study at 11 weeks of age. Members of the Clostridia, such as Blautia, Roseburia, and Anaerovibrio, were more abundant and part of the core microbiome in nonshedder pigs. Cellulolytic microbiota (Ruminococcus and Prevotella) were also more abundant in noninfected pigs during the weaning and growing stages. Microbial profiling also revealed that infected pigs had a higher abundance of Lactobacillus and Oscillospira, the latter also being part of the core microbiome of intermittent-persistent shedders. These findings suggest that a lack of microbiome maturation and greater proportions of microorganisms associated with suckling increase susceptibility to infection. In addition, the persistence of Salmonella shedding may be associated with an enrichment of pathobionts such as Anaerobiospirillum. Overall, these results suggest that there may be merit in manipulating certain taxa within the porcine intestinal microbial community to increase disease resistance against Salmonella in pigs. IMPORTANCE Salmonella is a global threat for public health, and pork is one of the main sources of human salmonellosis. However, the complex epidemiology of the infection limits current control strategies aimed at reducing the prevalence of this infection in pigs. The present study analyzes for the first time the impact of the gut microbiota in Salmonella infection in pigs and its shedding pattern in naturally infected growing pigs. Microbiome (16S rRNA amplicon) analysis reveals that maturation of the gut microbiome could be a key consideration with respect to limiting the infection and shedding of Salmonella in pigs. Indeed, seronegative animals had higher richness of the gut microbiota early after weaning, and uninfected pigs had higher abundance of strict anaerobes from the class Clostridia, results which demonstrate that a fast transition from the suckling microbiota to a postweaning microbiota could be crucial with respect to protecting the animals.

Item Type: Article
Additional Information: Funding Information: This study was funded by the Food Institutional Research Measure (FIRM) administered by the Department of Agriculture Food and the Marine (DAFM). H.A. is a postdoctoral researcher supported by the Juan de la Cierva Postdoctoral Trainee Program of the Spanish Ministry of Economy and Competitiveness (IJCI-2016-30795). H.A. was funded by the PiGutNet COST action (FA1401) for a Short-Term Scientific Mission at INRA?s GABI laboratory (Jouy-en-Josas, France). We gratefully acknowledge the Central Veterinary Research Laboratory (CVRL) Back-weston for their expert help with the serological analyses. H.A. participated in the study design, sample collection and processing, data analysis, and manuscript writing. F.C.L. participated in study design and manuscript correction. J.E. participated in data analysis and manuscript revision. P.D.C. and F.C. participated in microbiome sequencing and manuscript revision. O.O. performed part of the data analysis and manuscript revision. H.L. and K.W. participated in sample collection and processing. G.D. and P.G.L. participated in the study design and manuscript correction. G.E.G. participated in the study design, data analysis, and manuscript writing. Funding Information: This study was funded by the Food Institutional Research Measure (FIRM) administered by the Department of Agriculture Food and the Marine (DAFM). H.A. is a postdoctoral researcher supported by the Juan de la Cierva Postdoctoral Trainee Program of the Spanish Ministry of Economy and Competitiveness (IJCI-2016-30795). H.A. was funded by the PiGutNet COST action (FA1401) for a Short-Term Scientific Mission at INRA’s GABI laboratory (Jouy-en-Josas, France). Publisher Copyright: © 2019 Argüello et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license
Uncontrolled Keywords: /dk/atira/pure/subjectarea/asjc/2400/2404
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Depositing User: Admin SSL
Date Deposited: 19 Oct 2022 23:06
Last Modified: 01 Aug 2023 16:05
URI: http://repository-testing.wit.ie/id/eprint/4126

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