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Can probiotics improve the environmental microbiome and resistome of commercial poultry production?

ABSTRACT: Food animal production systems have become more consolidated and integrated, producing large, concentrated animal populations and significant amounts of fecal waste. Increasing use of manure and litter as a more "natural" and affordable source of fertilizer may be contributing to contamination of fruits and vegetables with foodborne pathogens. In addition, human and animal manure have been identified as a significant source of antibiotic resistance genes thereby serving as a disseminator of resistance to soil and waterways. Therefore, identifying methods to remediate human and animal waste is critical in developing strategies to improve food safety and minimize the dissemination of antibiotic resistant bacteria. In this study, we sought to determine whether withdrawing antibiotic growth promoters or using alternatives to antibiotics would reduce the abundance of antibiotic resistance genes or prevalence of pathogens in poultry litter. Terminal restriction fragment length polymorphism (T-RFLP) paired with high throughput sequencing was used to evaluate the bacterial community composition of litter from broiler chickens that were treated with streptogramin growth-promoting antibiotics, probiotics, or prebiotics. The prevalence of resistance genes and pathogens was determined from sequencing results or PCR screens of litter community DNA. Streptogramin antibiotic usage did not elicit statistically significant differences in Shannon diversity indices or correlation coefficients among the flocks. However, T-RFLP revealed that there were inter-farm differences in the litter composition that was independent of antibiotic usage. The litter from all farms, regardless of antibiotic usage, contained streptogramin resistance genes (vatA, vatB, and vatE), macrolide-lincosamide-streptogramin B resistance genes (ermA and ermB), the tetracycline resistance gene tetM and class 1 integrons. There was inter-farm variability in the distribution of vatA and vatE with no statistically significant differences with regards to usage. Bacterial diversity was higher in litter when probiotics or prebiotics were administered to flocks but as the litter aged, diversity decreased. No statistically significant differences were detected in the abundance of class 1 integrons where 3%-5% of the community was estimated to harbor a copy. Abundance of pathogenic Clostridium species increased in aging litter despite the treatment while the abundance of tetracycline-resistant coliforms was unaffected by treatment. However some treatments decreased the prevalence of Salmonella. These findings suggest that withdrawing antibiotics or administering alternatives to antibiotics can change the litter bacterial community and reduce the prevalence of some pathogenic bacteria, but may not immediately impact the prevalence of antibiotic resistance.

SUBMITTER: Pedroso AA

PROVIDER: S-EPMC3823317 | biostudies-literature | 2013 Oct

REPOSITORIES: biostudies-literature

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Can probiotics improve the environmental microbiome and resistome of commercial poultry production?

Pedroso Adriana A AA Hurley-Bacon Anne L AL Zedek Andrea S AS Kwan Tiffany W TW Jordan Andrea P O AP Avellaneda Gloria G Hofacre Charles L CL Oakley Brian B BB Collett Stephen R SR Maurer John J JJ Lee Margie D MD

International journal of environmental research and public health 20130925 10

Food animal production systems have become more consolidated and integrated, producing large, concentrated animal populations and significant amounts of fecal waste. Increasing use of manure and litter as a more "natural" and affordable source of fertilizer may be contributing to contamination of fruits and vegetables with foodborne pathogens. In addition, human and animal manure have been identified as a significant source of antibiotic resistance genes thereby serving as a disseminator of resi ...[more]

PMID: 24071920

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Project description:The microbiome profiles of poultry production systems significantly impact bird health, welfare, and the environment. This study investigated the influence of broiler-rearing systems on the microbiome composition of commercial and backyard chicken farms and their environment over time. Understanding these effects is vital for optimizing animal growth, enhancing welfare, and addressing human and environmental health implications. We collected and analyzed various samples from commercial and backyard farms, revealing significant differences in microbial diversity measurements between the two systems. Backyard farms exhibited higher alpha diversity measurements in soil and water samples, while commercial farms showed higher values for litter and feeder samples. The differences in microbial diversity were also reflected in the relative abundance of various microbial taxa. In backyard farms, Proteobacteria levels increased over time, while Firmicutes levels decreased. Campilobacterota, including the major poultry foodborne pathogen Campylobacter, increased over time in commercial farm environments. Furthermore, Bacteroides, associated with improved growth performance in chickens, were more abundant in backyard farms. Conversely, pathogenic Acinetobacter was significantly higher in backyard chicken fecal and feeder swab samples. The presence of Brevibacterium and Brachybacterium, associated with low-performing broiler flocks, was significantly higher in commercial farm samples. The observed differences in microbial composition and diversity suggest that farm management practices and environmental conditions significantly affect poultry health and welfare and have potential implications for human and environmental health. Understanding these relationships can inform targeted interventions to optimize poultry production, improve animal welfare, and mitigate foodborne pathogens and antimicrobial resistance risks. IMPORTANCE The microbiome of poultry production systems has garnered significant attention due to its implications on bird health, welfare, and overall performance. The present study investigates the impact of different broiler-rearing systems, namely, commercial (conventional) and backyard (non-conventional), on the microbiome profiles of chickens and their environment over time. Understanding the influence of these systems on microbiome composition is a critical aspect of the One-Health concept, which emphasizes the interconnectedness of animal, human, and environmental health. Our findings demonstrate that the type of broiler production system significantly affects both the birds and their environment, with distinct microbial communities associated with each system. This study reveals the presence of specific microbial taxa that differ in abundance between commercial and backyard poultry farms, providing valuable insights into the management practices that may alter the microbiome in these settings. Furthermore, the dynamic changes in microbial composition over time observed in our study highlight the complex interplay between the poultry gut microbiome, environmental factors, and production systems. By identifying the key microbial players and their fluctuations in commercial and backyard broiler production systems, this research offers a foundation for developing targeted strategies to optimize bird health and welfare while minimizing the potential risks to human and environmental health. The results contribute to a growing body of knowledge in the field of poultry microbiome research and have the potential to guide future improvements in poultry production practices that promote a sustainable and healthy balance between the birds, their environment, and the microbial communities they host.

Project description:While characterizing the intestinal bacterial community of broiler chickens, we detected epsilon-proteobacterial DNA in the ilea of 3-day-old commercial broiler chicks (J. Lu, U. Idris, B. Harmon, C. Hofacre, J. J. Maurer, and M. D. Lee, Appl. Environ. Microbiol. 69:6816-6824, 2003). The sequences exhibited high levels of similarity to Campylobacter jejuni and Campylobacter coli sequences, suggesting that chickens can carry Campylobacter at a very young age. Campylobacter sp. was detected by PCR in all samples collected from the ilea of chicks that were 3 to 49 days old; however, it was detected only in the cecal contents of chickens that were at least 21 days old. In order to determine whether the presence of Campylobacter DNA in young chicks was due to ingestion of the bacteria in food or water, we obtained commercial broiler hatching eggs, which were incubated in a research facility until the chicks hatched. DNA sequencing of the amplicons resulting from Campylobacter-specific 16S PCR performed with the ileal, cecal, and yolk contents of the day-of-hatching chicks revealed that Campylobacter DNA was present before the chicks consumed food or water. The 16S rRNA sequences exhibited 99% similarity to C. jejuni and C. coli sequences and 95 to 98% similarity to sequences of other thermophilic Campylobacter species, such as C. lari and C. upsaliensis. The presence of C. coli DNA was detected by specific PCR in the samples from chicks obtained from a commercial hatchery; however, no Campylobacter was detected by culturing. In order to determine whether the same strains of bacteria were present in multiple levels of the integrator, we cultured Campylobacter sp. from a flock of broiler breeders and their 6-week-old progeny that resided on a commercial broiler farm. The broiler breeders had been given fluoroquinolone antibiotics, and we sought to determine whether the same fluoroquinolone-resistant strain was present in their progeny. The isolates were typed by pulsed-field gel electrophoresis, which confirmed that the parental and progeny flocks contained the same strain of fluoroquinolone-resistant C. coli. These data indicate that resistant C. coli can be present in multiple levels of an integrated poultry system and demonstrated that molecular techniques or more sensitive culture methods may be necessary to detect early colonization by Campylobacter in broiler chicks.

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Can probiotics improve the environmental microbiome and resistome of commercial poultry production?

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Can probiotics improve the environmental microbiome and resistome of commercial poultry production?

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