The effect of the timing of exposure to Campylobacter jejuni on the gut microbiome and inflammatory responses of broiler chickens

Abstract

BackgroundCampylobacters are an unwelcome member of the poultry gut microbiota in terms of food safety. The objective of this study was to compare the microbiota, inflammatory responses, and zootechnical parameters of broiler chickens not exposed to Campylobacter jejuni with those exposed either early at 6 days old or at the age commercial broiler chicken flocks are frequently observed to become colonized at 20 days old.ResultsBirds infected with Campylobacter at 20 days became cecal colonized within 2 days of exposure, whereas birds infected at 6 days of age did not show complete colonization of the sample cohort until 9 days post-infection. All birds sampled thereafter were colonized until the end of the study at 35 days (mean 6.1 log10 CFU per g of cecal contents). The cecal microbiota of birds infected with Campylobacter were significantly different to age-matched non-infected controls at 2 days post-infection, but generally, the composition of the cecal microbiota were more affected by bird age as the time post infection increased. The effects of Campylobacter colonization on the cecal microbiota were associated with reductions in the relative abundance of OTUs within the taxonomic family Lactobacillaceae and the Clostridium cluster XIVa. Specific members of the Lachnospiraceae and Ruminococcaceae families exhibit transient shifts in microbial community populations dependent upon the age at which the birds become colonized by C. jejuni. Analysis of ileal and cecal chemokine/cytokine gene expression revealed increases in IL-6, IL-17A, and Il-17F consistent with a Th17 response, but the persistence of the response was dependent on the stage/time of C. jejuni colonization that coincide with significant reductions in the abundance of Clostridium cluster XIVa.ConclusionsThis study combines microbiome data, cytokine/chemokine gene expression with intestinal villus, and crypt measurements to compare chickens colonized early or late in the rearing cycle to provide insights into the process and outcomes of Campylobacter colonization. Early colonization results in a transient growth rate reduction and pro-inflammatory response but persistent modification of the cecal microbiota. Late colonization produces pro-inflammatory responses with changes in the cecal microbiota that will endure in market-ready chickens.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0477-5) contains supplementary material, which is available to authorized users.

Galacto-oligosaccharides modulate the juvenile gut microbiome and innate immunity to improve broiler chicken performance

“…The provision of dietary GOS increased the density of goblet cells populating ileal villi in the developing chicken gut. Goblet cell increases were accompanied by significant differences in the villus height and crypt depth at 15 da, a period when transitions in the development of the chicken microbiota from a juvenile to a mature composition are observed (70)(71)(72). Using molecular methods, we have demonstrated a significant correlation between the market weight of chickens at 35 da and the cecal abundance of a specific L. johnsonii isolate identified as differentially abundant in the juvenile microbiota of GOS-fed birds.…”

“…Reverse Transcription was performed with 1 g of RNA, SuperScript II (Invitrogen Life Technologies, Carlsbad, USA.) and random hexamers as described previously (70).…”

A mathematical model of Campylobacter dynamics within a broiler flock

“…This creates a brief window at 439 the point in which maternal antibodies have depleted, whereby any new strain 440 introduced is observed to quickly colonise and dominate the gut flora, suppressing other 441 strains (see Figure 10C). This hypothesis has been verified experimentally [39]. lower Campylobacter prevalence rate than commercial broiler flocks [41].…”

“…First, the most apparent prediction is that the Campylobacter population is successfully 430 suppressed by the innate maternal antibodies (an experimentally observed 431 phenomenon [39]), until these antibodies are eventually removed from the system. At Campylobacter to emerge as an early dominating strain.…”

Genetic control ofCampylobactercolonisation in broiler chickens: genomic and transcriptomic characterisation

“…Our pathway analysis also showed enrichment for other innate and adaptive immune related pathways in association with Campylobacter resistance. Of increased interest is the pathway related with IL-17 signalling since several previous studies suggested that IL-17 signalling and T H -17 responses play a role in resistance to Campylobacter colonisation in chickens following experimental inoculation [13, 16, 19, 56, 63, 64]. Future studies could seek to characterise the timing and magnitude of such responses in birds of predicted resistant or susceptible genotypes upon exposure.…”