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The Intestinal Microbiota Influences Campylobacter jejuni Colonization and Extraintestinal Dissemination in Mice.

ABSTRACT: Campylobacter jejuni is a leading cause of human foodborne gastroenteritis worldwide. The interactions between this pathogen and the intestinal microbiome within a host are of interest as endogenous intestinal microbiota mediates a form of resistance to the pathogen. This resistance, termed colonization resistance, is the ability of commensal microbiota to prevent colonization by exogenous pathogens or opportunistic commensals. Although mice normally demonstrate colonization resistance to C. jejuni, we found that mice treated with ampicillin are colonized by C. jejuni, with recovery of Campylobacter from the colon, mesenteric lymph nodes, and spleen. Furthermore, there was a significant reduction in recovery of C. jejuni from ampicillin-treated mice inoculated with a C. jejuni virulence mutant (?flgL strain) compared to recovery of mice inoculated with the C. jejuni wild-type strain or the C. jejuni complemented isolate (?flgL/flgL). Comparative analysis of the microbiota from nontreated and ampicillin-treated CBA/J mice led to the identification of a lactic acid-fermenting isolate of Enterococcus faecalis that prevented C. jejuni growth in vitro and limited C. jejuni colonization of mice. Next-generation sequencing of DNA from fecal pellets that were collected from ampicillin-treated CBA/J mice revealed a significant decrease in diversity of operational taxonomic units (OTUs) compared to that in control (nontreated) mice. Taken together, we have demonstrated that treatment of mice with ampicillin alters the intestinal microbiota and permits C. jejuni colonization. These findings provide valuable insights for researchers using mice to investigate C. jejuni colonization factors, virulence determinants, or the mechanistic basis of probiotics.

SUBMITTER: O'Loughlin JL

PROVIDER: S-EPMC4551207 | biostudies-literature | 2015 Jul

REPOSITORIES: biostudies-literature

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The Intestinal Microbiota Influences Campylobacter jejuni Colonization and Extraintestinal Dissemination in Mice.

O'Loughlin Jason L JL Samuelson Derrick R DR Braundmeier-Fleming Andrea G AG White Bryan A BA Haldorson Gary J GJ Stone Jennifer B JB Lessmann Jeremy J JJ Eucker Tyson P TP Konkel Michael E ME

Applied and environmental microbiology 20150501 14

Campylobacter jejuni is a leading cause of human foodborne gastroenteritis worldwide. The interactions between this pathogen and the intestinal microbiome within a host are of interest as endogenous intestinal microbiota mediates a form of resistance to the pathogen. This resistance, termed colonization resistance, is the ability of commensal microbiota to prevent colonization by exogenous pathogens or opportunistic commensals. Although mice normally demonstrate colonization resistance to C. jej ...[more]

PMID: 25934624

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Project description:BACKGROUND: Campylobacter jejuni causes enterocolitis in humans, but does not incite disease in asymptomatic carrier animals. To survive in the intestine, C. jejuni must successfully compete with the microbiota and overcome the host immune defense. Campylobacter jejuni colonization success varies considerably amongst individual mice, and we examined the degree to which the intestinal microbiota was affected in mice (i.e. a model carrier animal) colonized by C. jejuni at high relative to low densities. METHODS: Mice were inoculated with C. jejuni or buffer, and pathogen shedding and intestinal colonization were measured. Histopathologic scoring and quantification of mRNA expression for ?-defensins, toll-like receptors, and cytokine genes were conducted. Mucosa-associated bacterial communities were characterized by two approaches: multiplexed barcoded pyrosequencing and terminal restriction fragment length polymorphism analysis. RESULTS: Two C. jejuni treatments were established based on the degree of cecal and colonic colonization; C. jejuni Group A animals were colonized at high cell densities, and C. jejuni Group B animals were colonized at lower cell densities. Histological examination of cecal and colonic tissues indicated that C. jejuni did not incite visible pathologic changes. Although there was no significant difference among treatments in expression of mRNA for ?-defensins, toll-like receptors, or cytokine genes, a trend for increased expression of toll-like receptors and cytokine genes was observed for C. jejuni Group A. The results of the two methods to characterize bacterial communities indicated that the composition of the cecal microbiota of C. jejuni Group A mice differed significantly from C. jejuni Group B and Control mice. This difference was due to a reduction in load, diversity and richness of bacteria associated with the cecal mucosa of C. jejuni Group A mice. CONCLUSIONS: High density colonization by C. jejuni is associated with a dysbiosis in the cecal microbiota independent of prominent inflammation.

Project description:Human campylobacteriosis constitutes a zoonotic food-borne disease and a progressively rising health burden of significant socioeconomic impact. We have recently shown that conventional mice are protected from Campylobacter jejuni infection, which was not the case for human microbiota associated (hma) mice indicating that the host-specific gut microbiota composition primarily determines susceptibility to or resistance against C. jejuni infection. In our present preclinical intervention study we addressed whether gut microbiota changes in stably C. jejuni infected hma mice following murine fecal microbiota transplantation (mFMT) could alleviate pathogen-induced immune responses. To accomplish this, secondary abiotic C57BL/6 mice were generated by broad-spectrum antibiotic treatment, perorally reassociated with a complex human gut microbiota and challenged with C. jejuni by gavage. Seven days later C. jejuni infected hma mice were subjected to peroral mFMT on 3 consecutive days. Within a week post-mFMT fecal pathogenic burdens had decreased by two orders of magnitude, whereas distinct changes in the gut microbiota composition with elevated numbers of lactobacilli and bifidobacteria could be assessed. In addition, mFMT resulted in less C. jejuni induced apoptotic responses in colonic epithelia, reduced numbers of macrophages and monocytes as well as of T lymphocytes in the large intestinal mucosa and lamina propria and in less distinct intestinal pro-inflammatory cytokine secretion as compared to mock challenge. Strikingly, inflammation dampening effects of mFMT were not restricted to the intestinal tract, but could also be observed systemically as indicated by elevated serum concentrations of pro-inflammatory cytokines such as TNF-α, IL-12p70, and IL-6 in C. jejuni infected hma mice of the mock, but not the mFMT cohort. In conclusion, our preclinical mFMT intervention study provides evidence that changes in the gut microbiota composition which might be achieved by pre- or probiotic formulations may effectively lower intestinal C. jejuni loads, dampen both, pathogen-induced intestinal and systemic inflammatory sequelae and may represent a useful tool to treat continuous shedding of C. jejuni by asymptomatic carriers which is critical in the context of food production, hospitalization and immunosuppression.

Project description:IntroductionLactobacilli may prevent broilers from colonization with Campylobacter spp. and other gram-negative zoonotic bacteria through lactic acid production and modulation of the intestinal microbiota. This study evaluated the effects of daily intake of Lactiplantibacillus plantarum 256 (LP256) on Campylobacter jejuni (C. jejuni) loads in ceca and feces of C. jejuni challenged broilers, together with the changes in the gut microbiota.MethodsTwo experiments were conducted using the broilers Ross 308 (R-308; Experiment 1) for 42 days and Rowan Ranger broilers (RR; Experiment 2) for 63 days. The LP256 strain was administered either via silage inoculated with LP256 or direct supplementation in the drinking water. Concurrently, haylage as a forage similar to silage but without any inoculum was tested. C. jejuni loads in fecal matter and cecal content were determined by plate counts and qPCR, respectively. The cecal microbiota, in response to treatments and the challenge, were assessed by 16S rRNA sequencing.Results and discussionCulturing results displayed a significant reduction in C. jejuni colonization (2.01 log) in the silage treatment in comparison to the control at 1 dpi (day post-infection) in Experiment 1. However, no treatment effect on C. jejuni was observed at the end of the experiment. In Experiment 2, no treatment effects on C. jejuni colonization were found to be statistically significant. Colonization load comparison at the peak of infection (3 dpi) to that at the end of the trial (32 dpi) revealed a significant reduction in C. jejuni in all groups, regardless of treatment. Colonization dynamics of C. jejuni in the cecal samples analyzed by qPCR showed no difference between any of the treatments in Experiment 1 or 2. In both experiments, no treatment effects on the cecal microbiota were observed. However, proportional changes in the bacterial composition were observed after the C. jejuni challenge, suggesting that colonization affected the gut microbiota. Overall, the daily intake of LP256 was not effective in reducing C. jejuni colonization in either broiler type at the end of the rearing period and did not cause any significant changes in the birds' cecal microbiota composition.

Project description:Background Campylobacter (C.) species are the most common bacterial cause of foodborne diarrhea in humans. Despite colonization, most animals do not show clinical signs, making recognition of affected flocks and disruption of the infection chain before slaughter challenging. Turkeys are often cocolonized with C. jejuni and C. coli. To understand the pathogen-host-interaction in the context of two different Campylobacter species, we compared the colonization patterns and quantities in mono- and co-colonized female commercial turkeys. In three repeated experiments we investigated the impact on gut morphology, functional integrity, and microbiota composition as parameters of gut health at seven, 14, and 28 days post-inoculation. Results Despite successful Campylobacter colonization, clinical signs or pathological lesions were not observed. C. coli persistently colonized the distal intestinal tract and at a higher load compared to C. jejuni. Both strains were isolated from livers and spleens, occurring more frequently in C. jejuni- and co-inoculated turkeys. Especially in C. jejuni-positive animals, translocation was accompanied by local heterophil infiltration, villus blunting, and shallower crypts. Increased permeability and lower electrogenic ion transport of the cecal mucosa were also observed. A lower relative abundance of Clostridia UCG-014, Lachnospiraceae, and Lactobacillaceae was noted in all inoculated groups compared to controls. Conclusions In sum, C. jejuni affects gut health and may interfere with productivity in turkeys. Despite a higher cecal load, the impact of C. coli on investigated parameters was less pronounced. Interestingly, gut morphology and functional integrity were also less affected in co-inoculated animals while the C. jejuni load decreased over time, suggesting C. coli may outcompete C. jejuni. Since a microbiota shift was observed in all inoculated groups, future Campylobacter intervention strategies may involve stabilization of the gut microbiota, making it more resilient to Campylobacter colonization in the first place. Supplementary Information The online version contains supplementary material available at 10.1186/s13099-022-00508-x.

Dataset Information

The Intestinal Microbiota Influences Campylobacter jejuni Colonization and Extraintestinal Dissemination in Mice.

Publications

The Intestinal Microbiota Influences Campylobacter jejuni Colonization and Extraintestinal Dissemination in Mice.

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