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SteE Enhances the Virulence of Salmonella Pullorum in Chickens by Regulating the Inflammation Response

ABSTRACT: Salmonella enterica serovar Pullorum (S. Pullorum) is a host-specific pathogen, which causes acute gastroenteritis with high mortality in poultry. However, the association between steE, encoded by type III secretion system 2, and Salmonella virulence is not well-understood. To elucidate the functions of steE in S. Pullorum, ΔsteE strain was constructed using the λ-Red recombination technology. Compared to that in the wild-type, the deletion of steE in S. Pullorum reduced bacterial invasion, proliferation, and late apoptosis in the infected HD-11 cells. In addition, we analyzed the mRNA expression levels of effector genes and cytokines by qRT-PCR. SteE was associated with the regulation of various effector genes and inflammatory cytokines in HD-11 cells during S. Pullorum infection. The wild-type effector steE promoted the expression of anti-inflammatory cytokines (IL-4 and IL-10) and reduced that of pro-inflammatory cytokines (IL-1β, IL-6, and IL-12) compared to that in the ΔsteE-infected HD-11 cells and chicken spleens. Results from the chicken infection model showed that the deletion of steE resulted in significantly decreased colonization and long-term survival of the bacteria and alleviated pathological lesions compared to those in the wild-type. Further, steE increased the virulence of S. Pullorum in chickens by regulating the expression of inflammatory cytokines. Our findings provide insights into the persistent infection and autoimmunity associated with steE in S. Pullorum.

SUBMITTER: Liu Z

PROVIDER: S-EPMC9330158 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Pullorum disease is one of the most common diarrhea-related diseases caused by Salmonella enterica subspecies enterica serovar Gallinarum biovar Pullorum (S Pullorum); it negatively affects the poultry industry. However, limited studies have explored the association between the gut microbiota and S Pullorum infection in chickens. In the present study, we performed a microbiome comparison and a microbiome genome-wide association study (mGWAS) to investigate the association among the host genetics, the gut microbiota, and pullorum disease in chickens. We found that S Pullorum infection in chickens could alter the abundance of 39 bacterial genera (P < 0.05). The altered structure and composition of the gut microbiota were also detected in the offspring. mGWAS results revealed host genetic variants to be prominently associated with gut microbial diversity and individual microbes. The pathogens Pelomonas and Brevundimonas, which had a high abundance in positive parent chickens and their offspring, were significantly associated with several genetic mutations in immunity-related genes, such as TGIF1, TTLL12, and CCR7 This finding explained why Pelomonas and Brevundimonas were heritable in S Pullorum-infected chickens. The heritable gut microbes and identified genetic variants could provide references for the selection of resistant chickens and the elimination of pullorum disease.IMPORTANCE The present study investigated the association among the host genome, the gut microbiome, and S Pullorum infection in chickens. The results suggested that the gut microbial structure is altered in S Pullorum-infected chickens. The diversity and abundance of the gut microbiota remarkably differed between the offspring coming from S Pullorum-positive and S Pullorum-negative chickens. Heritable gut microbiota were detected in the offspring. Moreover, host genetic variants were associated with microbial diversity and individual gut microbes. The pathogens Pelomonas and Brevundimonas, which exhibited a high heritability in S Pullorum-positive parents and their offspring, were associated with several genetic mutations in immunity-related genes.

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SteE Enhances the Virulence of Salmonella Pullorum in Chickens by Regulating the Inflammation Response

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