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United States Department of Agriculture

Agricultural Research Service

Research Project: ANIMAL INTESTINAL MICROBIOMES, FOODBORNE PATHOGENS, AND ANTIMICROBIALS Title: Antibiotics in feed induce prophages in swine fecal microbiomes

Authors
item Allen, Heather
item Looft, Torey
item Bayles, Darrell
item Humphrey, Samuel
item Levine, Uri
item Alt, David
item Stanton, Thaddeus

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: November 3, 2011
Publication Date: November 29, 2011
Citation: Allen, H.K., Looft, T.P., Bayles, D.O., Humphrey, S.B., Levine, U.Y., Alt, D.P., Stanton, T.B. 2011. Antibiotics in feed induce prophages in swine fecal microbiomes. mBio [serial online]. 2(6). Available: http://mbio.asm.org/content/2/6/e00260-11.

Interpretive Summary: This study advances our knowledge of the collateral effects of in-feed antibiotics at a time in which the widespread use of “growth-promoting” antibiotics in agriculture is under scrutiny. Using comparative metagenomics, we show that prophages are induced by in-feed antibiotics in swine fecal microbiomes, and that antibiotic resistance genes were detected in most viromes. This demonstrates that in-feed antibiotics are contributing to phage-mediated gene transfer, potentially of antibiotic resistance genes, in the swine gut. Additionally, the so-called kill-the-winner model of phage-bacteria population dynamics has been shown in aquatic ecosystems, but met with conflicting evidence in gut ecosystems. Our data support that swine fecal Firmicutes bacteria and their phages follow the kill-the-winner model. Understanding the role of phages in gut microbial ecology is an essential component of the antibiotic resistance problem and of developing potential mitigation strategies.

Technical Abstract: Antibiotics are a cost-effective tool for improving feed-efficiency in agricultural animals, but the full scope of their collateral effects is not understood. Antibiotics have been shown to induce prophage-mediated gene transfer in certain bacterial strains; therefore, one collateral effect could be prophage induction in the gut microbiome at large. Here we used metagenomics to evaluate the effect of two in-feed antibiotics (carbadox and ASP250 [chlortetracycline, sulfamethazine, and penicillin]) on swine fecal phage metagenomes (viromes). We also monitored the bacterial community using 16S rRNA gene sequencing. ASP250, but not carbadox, caused significant population shifts in both the phage and bacterial communities. Antibiotic resistance genes, such as multidrug resistance efflux pumps, were identified in the viromes, but in-feed antibiotics caused no significant changes in their abundance. The abundance of integrase-encoding genes was significantly increased in the medicated versus non-medicated viromes, demonstrating the induction of prophages with antibiotic treatment. Phage-bacteria population dynamics were also examined. We observed a decrease in the abundance of Firmicutes bacteria (prey) when Firmicutes phages (predators) were abundant, supporting the “kill-the-winner” ecological model of population dynamics in the swine fecal microbiome. Our data show that gut ecosystem dynamics are influenced by phages, and that prophage induction is a collateral effect of in-feed antibiotics.

Last Modified: 7/23/2014
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