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      The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens

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          Abstract

          Background

          Poultry represent an important source of foodborne enteropathogens, in particular thermophilic Campylobacter species. Many of these organisms colonize the intestinal tract of broiler chickens as harmless commensals, and therefore, often remain undetected prior to slaughter. The exact reasons for the lack of clinical disease are unknown, but analysis of the gastrointestinal microbiota of broiler chickens may improve our understanding of the microbial interactions with the host.

          Methods

          In this study, the fecal microbiota of 31 market-age (56-day old) broiler chickens, from two different farms, was analyzed using high throughput sequencing. The samples were then screened for two emerging human pathogens, Campylobacter concisus and Helicobacter pullorum, using species-specific PCR.

          Results

          The gastrointestinal microbiota of chickens was classified into four potential enterotypes, similar to that of humans, where three enterotypes have been identified. The results indicated that variations between farms may have contributed to differences in the microbiota, though each of the four enterotypes were found in both farms suggesting that these groupings did not occur by chance. In addition to the identification of Campylobacter jejuni subspecies doylei and the emerging species, C. concisus, C. upsaliensis and H. pullorum, several differences in the prevalence of human pathogens within these enterotypes were observed. Further analysis revealed microbial taxa with the potential to increase the likelihood of colonization by a number of these pathogens, including C. jejuni.

          Conclusion

          Depletion of these taxa and the addition of taxa that compete with these pathogens, may form the basis of competitive exclusion strategies to eliminate them from the gastrointestinal tract of chickens.

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          Most cited references38

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          Modulations of the Chicken Cecal Microbiome and Metagenome in Response to Anticoccidial and Growth Promoter Treatment

          With increasing pressures to reduce or eliminate the use of antimicrobials for growth promotion purposes in production animals, there is a growing need to better understand the effects elicited by these agents in order to identify alternative approaches that might be used to maintain animal health. Antibiotic usage at subtherapeutic levels is postulated to confer a number of modulations in the microbes within the gut that ultimately result in growth promotion and reduced occurrence of disease. This study examined the effects of the coccidiostat monensin and the growth promoters virginiamycin and tylosin on the broiler chicken cecal microbiome and metagenome. Using a longitudinal design, cecal contents of commercial chickens were extracted and examined using 16S rRNA and total DNA shotgun metagenomic pyrosequencing. A number of genus-level enrichments and depletions were observed in response to monensin alone, or monensin in combination with virginiamycin or tylosin. Of note, monensin effects included depletions of Roseburia, Lactobacillus and Enterococcus, and enrichments in Coprococcus and Anaerofilum. The most notable effect observed in the monensin/virginiamycin and monensin/tylosin treatments, but not in the monensin-alone treatments, was enrichments in Escherichia coli. Analysis of the metagenomic dataset identified enrichments in transport system genes, type I fimbrial genes, and type IV conjugative secretion system genes. No significant differences were observed with regard to antimicrobial resistance gene counts. Overall, this study provides a more comprehensive glimpse of the chicken cecum microbial community, the modulations of this community in response to growth promoters, and targets for future efforts to mimic these effects using alternative approaches.
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            The clinical importance of emerging Campylobacter species.

            A growing number of Campylobacter species other than C. jejuni and C. coli have been recognized as emerging human and animal pathogens. Although C. jejuni continues to be the leading cause of bacterial gastroenteritis in humans worldwide, advances in molecular biology and development of innovative culture methodologies have led to the detection and isolation of a range of under-recognized and nutritionally fastidious Campylobacter spp., including C. concisus, C. upsaliensis and C. ureolyticus. These emerging Campylobacter spp. have been associated with a range of gastrointestinal diseases, particularly gastroenteritis, IBD and periodontitis. In some instances, infection of the gastrointestinal tract by these bacteria can progress to life-threatening extragastrointestinal diseases. Studies have shown that several emerging Campylobacter spp. have the ability to attach to and invade human intestinal epithelial cells and macrophages, damage intestinal barrier integrity, secrete toxins and strategically evade host immune responses. Members of the Campylobacter genus naturally colonize a wide range of hosts (including pets, farm animals and wild animals) and are frequently found in contaminated food products, which indicates that these bacteria are at risk of zoonotic transmission to humans. This Review presents the latest information on the role and clinical importance of emerging Campylobacter spp. in gastrointestinal health and disease.
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              Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs.

              The microbiota of an animal's intestinal tract plays a vital role in the animal's overall health. There is a surprising scarcity of information on the microbial diversity in the gut of livestock species such as cattle and swine. Here we describe a bacterial 16S-based tag-encoded FLX amplicon pyrosequencing (bTEFAP) method that we have developed as a high-throughput universal tool for bacterial diversity, epidemiology, and pathogen detection studies. This method will allow hundreds of samples to be run simultaneously but analyzed individually or as groups. To test this new methodology, we individually evaluated the bacterial diversity in the ileum of 21 pigs. Ubiquitous bacteria detected in the newly weaned pigs were Clostridium spp., Lactobacillus spp., and Helicobacter spp. Many of the pigs had surprisingly low concentrations of beneficial bacteria such as Bifidobacterium spp. Only four of the pigs were shown to be positive for Salmonella spp. using traditional culture methods. A total of eight pigs were bTEFAP positive for Salmonella spp., including all four of the pigs that had been culture positive. Two of the pigs sampled were also positive for Campylobacter spp. tentative identified as jejuni. Using rarefaction curves modeled with the Richards equation, we estimated the maximum number of unique species level (3% dissimilarity) operational taxonomic units in the ileum of these pigs. These predictions indicated that there may be as many as 821 different species associated with the ileum in pigs. Together these data indicate a powerful potential of this technology in food safety and epidemiological and bacterial diversity applications. Using bTEFAP, we can expect to gain a better understanding of how the microbiome of an animal contributes to its health and well-being.
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                Author and article information

                Contributors
                Journal
                Gut Pathog
                Gut Pathog
                Gut Pathogens
                BioMed Central
                1757-4749
                2014
                4 June 2014
                : 6
                : 18
                Affiliations
                [1 ]School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, NSW 2052, Australia
                [2 ]Birling Avian Laboratories, Bringelly, NSW 2556, Australia
                [3 ]Faculty of Science, The University of New South Wales, Sydney, NSW 2052, Australia
                [4 ]Gastrointestinal and Liver Unit, The Prince of Wales Hospital, Randwick, NSW 2031, Australia
                [5 ]Prince of Wales Clinical School, The University of New South Wales, Sydney, NSW 2052, Australia
                Article
                1757-4749-6-18
                10.1186/1757-4749-6-18
                4060860
                24940386
                861fe1a0-b8af-4914-a81e-cec401afc900
                Copyright © 2014 Kaakoush et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 7 May 2014
                : 30 May 2014
                Categories
                Research

                Gastroenterology & Hepatology
                broiler chicken,gastrointestinal tract,microbiota,pathogen,campylobacter,helicobacter,gallibacterium,campylobacter concisus

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