Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin

Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 09/2012; 109(38):15485-90. DOI: 10.1073/pnas.1205147109
Source: PubMed


Antimicrobials have been used extensively as growth promoters (AGPs) in agricultural animal production. However, the specific mechanism of action for AGPs has not yet been determined. The work presented here was to determine and characterize the microbiome of pigs receiving one AGP, tylosin, compared with untreated pigs. We hypothesized that AGPs exerted their growth promoting effect by altering gut microbial population composition. We determined the fecal microbiome of pigs receiving tylosin compared with untreated pigs using pyrosequencing of 16S rRNA gene libraries. The data showed microbial population shifts representing both microbial succession and changes in response to the use of tylosin. Quantitative and qualitative analyses of sequences showed that tylosin caused microbial population shifts in both abundant and less abundant species. Our results established a baseline upon which mechanisms of AGPs in regulation of health and growth of animals can be investigated. Furthermore, the data will aid in the identification of alternative strategies to improve animal health and consequently production.

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Available from: Srinand Sreevatsan, May 02, 2014
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    • "Similarly, Kim et al. (2012) documented no difference at the bacterial phylum or class levels in 10 pigs continuously fed either tylosin (44 mg·(kg feed) −1 ) or a control, antibiotic-free diet, for 12 weeks starting at 10 weeks of age. These researchers sequenced the V3 region of the 16S rRNA gene using 454 pyrosequencing (Kim et al. 2012). There were also no identifiable changes in bacterial richness and diversity or in community structure metrics, although the swine gut microbiota may have already been well established and relatively stable at this stage of production (>10 weeks). "
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    ABSTRACT: Antimicrobials have been used in swine production at subtherapeutic levels since the early 1950s to increase feed efficiency and promote growth. In North America, a number of antimicrobials are available for use in swine. However, the continuous administration of subtherapeutic, low concentrations of antimicrobials to pigs also provides selective pressure for antimicrobial-resistant bacteria and resistance determinants. For this reason, subtherapeutic antimicrobial use in livestock remains a source of controversy and concern. The swine gut microbiota demonstrates a number of changes in response to antimicrobial administration depending on the dosage, duration of treatment, age of the pigs, and gut location that is sampled. Both culture-independent and dependent studies have also shown that the swine gut microbiota contains a large number of antimicrobial resistance determinants even in the absence of antimicrobial exposure. Heavy metals, such as zinc and copper, which are often added at relatively high doses to swine feed, may also play a role in maintaining antimicrobial resistance and on the stability of the swine gut microbiota. This review focuses on the use of antimicrobials in swine production, with an emphasis on the North American regulatory context, and their effect on the swine gut microbiota and on antimicrobial resistance determinants in the gut microbiota
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    • "It is generally hypothesized that the altered gut microflora in response to in-feed use leads to improvement in growth and efficiency of feed utilization. Additionally, antimicrobials also could act by inhibiting the growth of opportunistic gut pathogens in animals (Kim et al., 2012). Copper promotes growth of piglets independently of growth promotion by antibiotics (Cromwell et al., 1998). "
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    ABSTRACT: Heavy metals, such as copper, are increasingly supplemented in swine diets as an alternative to antibiotics to promote growth. Enterococci, a common gut commensal, acquire plasmid-borne, transferable copper resistance (tcrB) gene-mediated resistance to copper. The plasmid also carried resistance genes to tetracyclines and macrolides. The potential genetic link between copper and antibiotic resistance suggests that copper supplementation may exert a selection pressure for antimicrobial resistance. Therefore, a longitudinal study was conducted to investigate the effects of in-feed copper, chlortetracycline, and tylosin alone or in combination on the selection and co-selection of antimicrobial-resistant enterococci. The study included 240 weaned piglets assigned randomly to 6 dietary treatment groups: control, copper, chlortetracycline, tylosin, copper and chlortetracycline, and copper and tylosin. Feces were collected before (day 0), during (days 7, 14, 21), and after (days 28 and 35) initiating treatment, and enterococcal isolates were obtained from each fecal sample and tested for genotypic and phenotypic resistance to copper and antibiotics. A total of 2592 enterococcal isolates were tested for tcrB by polymerase chain reaction. The overall prevalence of tcrB-positive enterococci was 14.3% (372/2592). Among the tcrB-positive isolates, 331 were Enterococcus faecium and 41 were E. faecalis. All tcrB-positive isolates contained both erm(B) and tet(M) genes. The median minimum inhibitory concentration of copper for tcrB-negative and tcrB-positive enterococci was 6 and 18 mM, respectively. The majority of isolates (95/100) were resistant to multiple antibiotics. In conclusion, supplementing copper or antibiotics alone did not increase copper-resistant enterococci; however, supplementing antibiotics with copper increased the prevalence of the tcrB gene among fecal enterococci of piglets.
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    • "However, the results were limited to organisms with high copy numbers, including Firmicutes, Bacteroidetes, methanogens, and sulfate-reducing bacteria; thus, the ability to characterize the overall microbial composition was limited. High-throughput pyrosequencing methods have enabled researchers to generate a massive amount of data for community analyses to describe the effect of weaning (Pajarillo et al., 2014b), age (Kim et al., 2011), diet (Lu et al., 2013), and antibiotics (Kim et al., 2012) on the swine gut microbiome. Here, we describe the fecal bacterial diversity among Duroc pigs using 16S rRNA gene pyrosequencing and suggest core members of the microbial community, as well as uncultivable members of the adult Duroc gut microbiota. "
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    ABSTRACT: This study characterized the fecal bacterial community structure and inter-individual variation in 30-week-old Duroc pigs, which are known for their excellent meat quality. Pyrosequencing of the V1–V3 hypervariable regions of the 16S rRNA genes generated 108,254 valid reads and 508 operational taxonomic units at a 95% identity cut-off (genus level). Bacterial diversity and species richness as measured by the Shannon diversity index were significantly greater than those reported previously using denaturation gradient gel electrophoresis; thus, this study provides substantial information related to both known bacteria and the untapped portion of unclassified bacteria in the population. The bacterial composition of Duroc pig fecal samples was investigated at the phylum, class, family, and genus levels. Firmicutes and Bacteroidetes predominated at the phylum level, while Clostridia and Bacteroidia were most abundant at the class level. This study also detected prominent inter-individual variation starting at the family level. Among the core microbiome, which was observed at the genus level, Prevotella was consistently dominant, as well as a bacterial phylotype related to Oscillibacter valericigenes, a valerate producer. This study found high bacterial diversity and compositional variation among individuals of the same breed line, as well as high abundance of unclassified bacterial phylotypes that may have important functions in the growth performance of Duroc pigs.
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