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Lactobacillus casei protects intestinal mucosa from damage in chicks caused by Salmonella pullorum via regulating immunity and the Wnt signaling pathway and maintaining the abundance of gut microbiota.

ABSTRACT: Dysfunction of the intestinal mucosal barrier of chicks caused by Salmonella pullorum is of great harm to the poultry industry. Probiotics are recognized for their beneficial health-promoting properties, promoting maintenance of bowel epithelial integrity and host immune system homeostasis. Our previous research showed that Lactobacillus casei protects jejunal mucosa from injury in chicks infected with S. pullorum. However, the specific mechanisms underlying its protective properties are still not fully understood. In the present study, we aimed to explore the mechanisms underlying the protective effects of L. casei on the intestinal mucosal barrier of chicks infected with S. pullorum through histological, immunological, and molecular biology methods. The results indicated that L. casei significantly reduced the diarrhea rate, increased the daily weight gain, and maintained normal levels of IgA, IgM, and IgG in the serum of chicks infected with S. pullorum. Furthermore, we found that L. casei markedly improved the immunity of gut mucosa by regulating cytokine and chemokine receptor balance, elevating the number of intraepithelial lymphocytes, and hence effectively restraining bowel inflammation. Strikingly, feeding of infected chicks with L. casei notably boosted interleukin-22 expression to activate the Wingless-Int pathway, moderated diamine oxidase and D-lactic acid levels, diminished the generation of myosin light chain kinase, and expanded tight junction protein levels (Zonulin-1 and Claudin-1), strengthening the function of the gut mucosal epithelium. In addition, experiments using 16S rDNA sequencing also demonstrated that L. casei immensely weakened the adhesion of S. pullorum, mainly manifesting as improved diversity of the intestinal microbiota in the V4 area of infected chicks. Taken together, these results show that the application of L. casei may be a good strategy to regulate the intestinal inflammatory response of chicks infected with S. pullorum, providing new perspectives in producing antibiotic substitutes in poultry farms.

SUBMITTER: Deng Z

PROVIDER: S-EPMC8261010 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Pullorum disease caused by Salmonella Pullorum remains an important disease for the poultry industry due to high morbidity and mortality in many countries. Phage therapy is becoming an alternative strategy to control multidrug-resistant Salmonella infections in young chicks. However, how bacteriophages affect the growth performance of chicks infected with S. Pullorum remains poorly understood. Herein, we assessed the therapeutic efficacy of Salmonella phage CKT1 against hypervirulent arthritis-causing S. Pullorum. The results showed that single phage treatment after hypervirulent S. Pullorum infection significantly improved body weight loss of chicks. Compared with enlarged liver and spleen in only Salmonella challenged group, phage administration substantially reduced the liver/body and spleen/body weight ratios, bacterial loads in organs and the degree of hepatic sinusoidal dilatation and congestion. Moreover, phage CKT1 can enter the organs of chicks and stay for at least 3 d in liver and spleen, and promote higher serum levels of IL-6 production within 6 d postinfection, indicating phage-induced bacterial lysis may be involved in inflammatory immune response to S. Pullorum infection. Analysis of the microbiome of gastrointestinal tract of chicks demonstrated that Salmonella challenge significantly reduced the relative abundances of Lachnoclostridium and Blautia, resulting in remarkably increased Escherichia-Shigella and Klebsiella becoming the predominant bacterial taxa. In contrast, the use of phage CKT1 significantly reduced Escherichia-Shigella and Klebsiella populations in intestine, permitting the proliferation of beneficial microbiota in Firmicutes including Lachnoclostridium, Ruminococcus, Lactobacillus, and Pseudoflavonifractor. In addition, phage alone treatments did not affect the normal gut microbiota structure of chicks, and phage therapy on Salmonella infected chicks increased bacteria species richness in the cecum. These results suggest that Salmonella phage CKT1 could improve growth performance of chicks challenged with S. Pullorum by normalizing the abnormal intestinal microbiome.

Project description:Salmonella pullorum is a highly pathogenic bacteria in poultry industry. However, antibiotics were restricted in many countries because of the increasing risk of antibiotic resistance, Therefore, an environmental friendly and effective alternative strives to be developed. This study investigated the benefit of a probiotic-fermented herbal blend on the growth performance and gut microbiota of newborn broilers infected with S. pullorum. A total of 120 one-day-old dwarf male chicks were randomly allotted to 4 treatment groups, each including 5 replicates of 6 chicks: negative control (NC), positive control (PC), herbal blend (HB), and probiotic-fermented herbal blend (PF). All birds (n = 90), except for those in the NC, were infected with S. pullorum (1.69 × 108 CFU) on day 1. On day 11, body weight (BW), mortality, tissue pathology, cecal colony counts, immune organ indices, cecal mucosa secretory immunoglobulin A (sIgA) concentrations, and cecal cytokine mRNA expression levels were investigated. No mortality was observed after the PF treatment, and less pathological condition was in the ileum, cecum, and liver of HB and PF. BW, average daily gain and average daily feed intake were significant higher in the HB group compared to the PC and were the highest in the PF (P < 0.05). HB treatment significantly increased cecal populations of Lactobacilli, and decreased cecal populations of Escherichia coli and Salmonella, but results were more pronounced in the PF group (P < 0.05). Both HB and PF treatments increased cecal mucosa sIgA compared with the PC (P < 0.05). Tumor necrosis factor alpha and interferon gamma were lowest (P < 0.05) and interleukin 4 was the highest (P < 0.05) in PF, which exhibited similar levels to the NC group. PF treatment significantly improved the development of the thymus and bursa in S. pullorum-infected chicks. In conclusion, PF treatment prevented death, improved growth performance, regulated intestinal flora and enhanced immune ability of in S. pullorum-infected with chicks.

Project description:Reactive arthritis is the development of sterile joint inflammation as a sequel to a remote infection, often in the gut. We have previously shown that a low dose of S. enteritidis inoculated to streptomycin-pretreated mice generates a self-limiting enterocolitis suitable for studying reactive arthritis. Here we show that consumption of Lactobacillus casei prior to infection abolishes intestinal and joint inflammation triggered by Salmonella. BALB/c mice were sacrificed after infection; intestinal and joint samples were analyzed for histological changes and expression of cytokines. TNF-α was measured by ELISA and the expression of IL-1β, IL-6, IL-10, IL-17, IL-23 and TGF-β was assessed by qPCR. L. casei consumption prevented Salmonella-induced synovitis, the increment of TNF-α in knees and the increase of IL-17 expression in popliteal and inguinal lymph nodes. At intestinal level consumption of L. casei drastically diminished S. enteritidis invasiveness and shortened splenic persistence of the pathogen. Bacterial loads recovered at days 2 and 5 from Peyer's patches were 10-fold lower in mice fed with L. casei. In accordance, we found that the augment in gut permeability induced during enterocolitis was decreased in those animals. Consumption of L. casei prior to infection failed to increase anti- inflammatory molecules such as IL-10 and TGF-β in the intestine. On the other hand, consumption of L. casei abrogated the expression of TNF-α, IL-17, IL-23, IL-1β and IL-6 in cecum and mesenteric lymph nodes. These cytokines are needed for differentiation of immune cells involved in the development of reactive arthritis such as Th17 and γδ T cells. Trafficking of these inflammatory cells from the gut to the joints has been proposed as a mechanism of generation of reactive arthritis. Our results suggest that L. casei consumption prevents Salmonella-induced synovitis by altering the intestinal milieu necessary for differentiation of cells involved in the generation of joint inflammation.

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Lactobacillus casei protects intestinal mucosa from damage in chicks caused by Salmonella pullorum via regulating immunity and the Wnt signaling pathway and maintaining the abundance of gut microbiota.

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