Influence of the Intestinal Microbiota on Colonization Resistance to Salmonella and the Shedding Pattern of Naturally Exposed Pigs

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.

Transport to the Slaughterhouse Affects the Salmonella Shedding and Modifies the Fecal Microbiota of Finishing Pigs

“…In fact, we have described an increased abundance of Prevotella, Coprococcus, and Paraprevotella in Salmonella-positive animals, which is in accordance with studies carried out in experimental Salmonella challenges [9,12,45]. Moreover, the fecal microbiota of negative pigs showed a higher abundance of Ruminococcaceae compared to the Salmonella-positive pigs, which is also in accordance with the literature [8,9,11]. Interestingly, our results showed that Salmonella-positive pigs had higher beta diversity compared with negative animals, meaning that Salmonella-positive pigs had more heterogeneous gut microbiota.…”

“…Overall, we observed that the phyla Bacteroidetes and Firmicutes were dominant in the fecal microbiota of finishing pigs. These two taxa accounted for 90% of all the sequences obtained, like in prior studies examining the gut microbiota of pigs [8,9,11,[38][39][40]. Moreover, the fecal core microbiota we uncovered was consistent with previous studies in pigs [41][42][43][44].…”

“…It is well-established that Salmonella infection affects the gut microbiota of pigs [8,9,11,12]. Overall, we observed that the phyla Bacteroidetes and Firmicutes were dominant in the fecal microbiota of finishing pigs.…”

“…Globally, our study and the cited studies clearly demonstrate that Salmonella leads to alterations in the composition of the pig gut microbiota either on the farm or in experimental conditions [8,9,11]. Nevertheless, we did not show a correlation in the fecal microbiota composition on the farm of the 'will-be' high-shedder pigs at slaughter.…”

“…Most studies described a disruption of the porcine gut microbiota as a consequence of Salmonella infection [8][9][10]. A higher abundance of the family Ruminococcaceae in Salmonella-negative or low-shedder pigs and depletion of Prevotella in high-shedder pigs early after the infection was reported [10][11][12]. However, the majority of these investigations were carried out in challenge studies, which may not reflect the conditions occurring during a natural infection.…”