Composition of diet modifies colonization dynamics of<i>Campylobacter jejuni</i>in broiler chickens

Molnár, Andor; Heß, Claudia; Pál, László; Wagner, László; Awad, W. A.; Húsvéth, Ferenc; Heß, Michael; Dublecz, Károly

doi:10.1111/jam.12679

Cited by 37 publications

(38 citation statements)

References 35 publications

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“…Acetate is an SCFA metabolite produced as a by-product by commensal bacteria and is most abundantly found in the lower intestinal tracts of many hosts, including avian species (29, 30). Other SCFAs, such as butyrate and propionate, are also produced by commensals and commonly found in the same intestinal regions as acetate.…”

Section: Resultsmentioning

confidence: 99%

Microbiota-Derived Short-Chain Fatty Acids Modulate Expression of Campylobacter jejuni Determinants Required for Commensalism and Virulence

Luethy

Huynh

Ribardo

et al. 2017

mBio

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Campylobacter jejuni promotes commensalism in the intestinal tracts of avian hosts and diarrheal disease in humans, yet components of intestinal environments recognized as spatial cues specific for different intestinal regions by the bacterium to initiate interactions in either host are mostly unknown. By analyzing a C. jejuni acetogenesis mutant defective in converting acetyl coenzyme A (Ac-CoA) to acetate and commensal colonization of young chicks, we discovered evidence for in vivo microbiota-derived short-chain fatty acids (SCFAs) and organic acids as cues recognized by C. jejuni that modulate expression of determinants required for commensalism. We identified a set of C. jejuni genes encoding catabolic enzymes and transport systems for amino acids required for in vivo growth whose expression was modulated by SCFAs. Transcription of these genes was reduced in the acetogenesis mutant but was restored upon supplementation with physiological concentrations of the SCFAs acetate and butyrate present in the lower intestinal tracts of avian and human hosts. Conversely, the organic acid lactate, which is abundant in the upper intestinal tract where C. jejuni colonizes less efficiently, reduced expression of these genes. We propose that microbiota-generated SCFAs and lactate are cues for C. jejuni to discriminate between different intestinal regions. Spatial gradients of these metabolites likely allow C. jejuni to locate preferred niches in the lower intestinal tract and induce expression of factors required for intestinal growth and commensal colonization. Our findings provide insights into the types of cues C. jejuni monitors in the avian host for commensalism and likely in humans to promote diarrheal disease.

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Section: Resultsmentioning

confidence: 99%

Microbiota-Derived Short-Chain Fatty Acids Modulate Expression of Campylobacter jejuni Determinants Required for Commensalism and Virulence

Luethy

Huynh

Ribardo

et al. 2017

mBio

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“…This link can also be explained by the fact that the Clostridium organic acid production could be used by C. jejuni as an energy source. Furthermore, it was found that a Campylobacter infection induces excess mucous production in the intestine (Molnár et al, 2015) which consequently may enhance Clostridium proliferation due to the fact that an increase in mucin secretion in the gut provides an opportunity for Clostridium spp. to proliferate (M'Sadeq et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Age-Related Differences in the Luminal and Mucosa-Associated Gut Microbiome of Broiler Chickens and Shifts Associated with Campylobacter jejuni Infection

Awad¹,

Mann

Dzieciol

et al. 2016

Front. Cell. Infect. Microbiol.

137

123

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Despite the importance of gut microbiota for broiler performance and health little is known about the composition of this ecosystem, its development and response towards bacterial infections. Therefore, the current study was conducted to address the composition and structure of the microbial community in broiler chickens in a longitudinal study from day 1 to day 28 of age in the gut content and on the mucosa. Additionally, the consequences of a Campylobacter (C.) jejuni infection on the microbial community were assessed. The composition of the gut microbiota was analyzed with 16S rRNA gene targeted Illumina MiSeq sequencing. Sequencing of 130 samples yielded 51,825,306 quality-controlled sequences, which clustered into 8285 operational taxonomic units (OTUs; 0.03 distance level) representing 24 phyla. Firmicutes, Proteobacteria, Bacteroidetes, Actinobacteria, and Tenericutes were the main components of the gut microbiota, with Proteobacteria and Firmicutes being the most abundant phyla (between 95.0 and 99.7% of all sequences) at all gut sites. Microbial communities changed in an age-dependent manner. Whereas, young birds had more Proteobacteria, Firmicutes, and Tenericutes dominated in older birds (>14 days old). In addition, 28 day old birds had more diverse bacterial communities than young birds. Furthermore, numerous significant differences in microbial profiles between the mucosa and luminal content of the small and large intestine were detected, with some species being strongly associated with the mucosa whereas others remained within the luminal content of the gut. Following oral infection of 14 day old broiler chickens with 1 × 108 CFU of C. jejuni NCTC 12744, it was found that C. jejuni heavily colonized throughout the small and large intestine. Moreover, C. jejuni colonization was associated with an alteration of the gut microbiota with infected birds having a significantly lower abundance of Escherichia (E.) coli at different gut sites. On the contrary, the level of Clostridium spp. was higher in infected birds compared with birds from the negative controls. In conclusion, the obtained results demonstrate how the bacterial microbiome composition changed within the early life of broiler chickens in the gut lumen and on the mucosal surface. Furthermore, our findings confirmed that the Campylobacter carrier state in chicken is characterized by multiple changes in the intestinal ecology within the host.

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“…Changing poultry diet may modify the caecal microbiota and gut health of chicken, and therefore may affect the colonization pattern of C. jejuni [11, 12]. Recent studies have shown that maize- or wheat-based diets, which contain different levels of crude protein, can alter the viscosity of gut content and histomorphology of the chicken gut [11], and subsequently reduce C. jejuni colonization in broilers [9].…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have shown that maize- or wheat-based diets, which contain different levels of crude protein, can alter the viscosity of gut content and histomorphology of the chicken gut [11], and subsequently reduce C. jejuni colonization in broilers [9]. Changes in diet due to different protein sources or non-antibiotic feed additive may modify the gastrointestinal environment creating disturbances in the resident microbiota thus allowing—directly or indirectly—either a proliferation or reduction of bacterial pathogens [10, 55].…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have shown that the feeding strategy can alter the viscosity of gut content as well as the histomorphology of the chicken gut [11], and modify goblet cell glycoconjugates in the intestinal tract in vitro [29]. It is not fully clear how different feeding strategies may alter the colonization pattern of the intestinal bacteria, the development of local immunity and subsequently modulate local immune reactions in response to C. jejuni colonization.…”

Section: Introductionmentioning

confidence: 99%

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Differences in host breed and diet influence colonization by Campylobacter jejuni and induction of local immune responses in chicken

Han¹,

Willer²,

Pielsticker³

et al. 2016

Gut Pathog

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BackgroundChickens are regarded as the main reservoir for human campylobacteriosis. Little is known about the interaction between Campylobacter jejuni (C. jejuni) and chickens. This interaction may be influenced by the stage of maturation of the immune system, developing gut microbiota composition and other factors including breed and diet. Our aim was to investigate the impact of breed, and diet on C. jejuni colonization and host immune responses in chickens. Birds were inoculated with 104 colony forming units (CFU) of C. jejuni or diluent at one (Exp. 1) or 22 (Exp. 2) days post hatch. We compared local immune cell subpopulations, cytokine expression levels, and gut microbiota composition between broiler-type (BT) and layer-type (LT) birds fed with either commercial broiler feed (bf) or layer feed (lf).ResultsLower colonization rates were observed in the older age group independent of breed and diet. Independent of breed, birds fed with bf showed higher CFU of C. jejuni compared to lf-fed groups. Campylobacter jejuni-inoculation had a significant effect on lymphocyte numbers and cytokine expression levels in BT birds independent of feeding strategy (p < 0.05). These effects were not detected in LT birds, only LT birds fed with bf showed a significant increase in IL-8-expression at 7 days post C. jejuni inoculation compared to LT-control birds (p < 0.05). Diet influenced gut microbiota composition in a comparable manner between BT and LT birds, but changes in microbiota composition associated with C. jejuni inoculation varied between breeds.ConclusionsDiet and breed influenced C. jejuni colonization, immune responses and microbiota composition to a different extent comparing between LT and BT birds. The mechanisms behind these differences have to be elucidated further. Our results suggest that selection for more resistant breeds in combination with adapted feeding strategies may help to reduce Campylobacter colonization levels in commercial poultry in the future.

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Composition of diet modifies colonization dynamics ofCampylobacter jejuniin broiler chickens

Abstract: Our study proves that diet composition can modify Camp. jejuni colonization depending on sampling time point postinfection.

Cited by 37 publications

References 35 publications

Microbiota-Derived Short-Chain Fatty Acids Modulate Expression of Campylobacter jejuni Determinants Required for Commensalism and Virulence

Microbiota-Derived Short-Chain Fatty Acids Modulate Expression of Campylobacter jejuni Determinants Required for Commensalism and Virulence

Age-Related Differences in the Luminal and Mucosa-Associated Gut Microbiome of Broiler Chickens and Shifts Associated with Campylobacter jejuni Infection

Differences in host breed and diet influence colonization by Campylobacter jejuni and induction of local immune responses in chicken

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