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ARS Home » Pacific West Area » Davis, California » Western Human Nutrition Research Center » Immunity and Disease Prevention Research » Research » Publications at this Location » Publication #354463

Title: The fecal resistome of dairy cattle is associated with diet during nursing

item LIU, JINXIN - University Of California, Davis
item TAFT, DIANA - University Of California, Davis
item GOMEZ, MARIA - University Of California, Davis
item JOHNSON, DAISY - University Of California, Davis
item TREIBER, MICHELLE - University Of California, Davis
item Lemay, Danielle
item DEPETERS, EDWARD - University Of California, Davis
item MILLS, DAVID - University Of California, Davis

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/24/2019
Publication Date: 9/27/2019
Citation: Liu, J., Taft, D.H., Gomez, M.X., Johnson, D., Treiber, M.L., Lemay, D.G., Depeters, E., Mills, D.A. 2019. The fecal resistome of dairy cattle is associated with diet during nursing. Nature Communications.

Interpretive Summary: Resistance of microbes to antibiotics is a growing concern for human health. After exposure to antibiotics, livestock such as cattle become a reservoir for microbes that have survived antibiotics and now harbor genes which confer antimicrobial resistance. The purpose of this study was to catalog and quantify antimicrobial resistance genes in beef and dairy cattle during early life and to investigate the contributors of diet to antimicrobial resistance in these animals. Dairy calves harbored more antibiotic resistance genes than beef calves. In dairy calves, colostrum was predicted to be the source of over 90% of antibiotic resistance genes. Functional analyses of stool metagenomes—all microbial DNA in the stool—was consistent with feeding of milk replacer and introduction of oat starter. These dietary changes correlated with a decrease in antimicrobial resistance genes as dominant species transitioned from Escherichia coli to more favorable species of the family Bacteroidaceae, which are naturally less antibiotic resistant. However, some medically important antimicrobial resistance genes increased over time. These findings imply that new dietary management practices are needed to promote the growth of taxa that are naturally lower in antimicrobial resistance genes to reduce the prevalence of antimicrobial resistance in dairy cattle.

Technical Abstract: Background: The increasing prevalence of antimicrobial resistance is a global concern to public health, and commensal bacteria could serve as critical reservoirs of antimicrobial resistance genes (ARGs). Livestock (e.g. cattle), which consume much more antibiotics than humans, play a significant role in selecting for antimicrobial resistance and maintaining such reservoirs. Antibiotic-resistant bacteria usually present an age-dependent distribution in cattle in which pre-weaned calves harbor the highest abundance of resistance. Despite this, knowledge of the ARGs possessed by commensal bacteria and the resistome structure in cattle remains limited, and the relationship between the succession of resistome and the assembling bovine gut microbiome during early life is yet unclear. Results: The intestinal microbiome assembled rapidly in bovine calves. Beef and dairy animals possessed remarkably different fecal microbiota profiles as well as the microbial communities observed in colostrum. While dairy calves had a less diverse fecal community than beef calves they possessed a significantly higher abundance of ARGs. Specifically, a total of 329 ARGs conferring resistance to 17 classes of antibiotics were observed in dairy calves with Enterobacteriaceae predicted to harbor the most transferrable ARGs. The abundance of total ARGs greatly reduced during nursing, however, some clinically relevant ARGs which encode resistance to macrolides-lincosamides-streptogramines and tetracyclines increased throughout this period. Network modeling indicated that ARGs in dairy calves co-occur with antibacterial biocide/metal resistance genes. Colostrum was predicted to be the source of over 90% of ARGs observed in dairy calves at day 2. The early succession of resistome is a result of gut microbiome assembly which is likely driven by the diet transition in dairy calves. This is suggested by the fact that carbohydrates-associated enzymes (e.g. lactase), which are more prevalent during early days than later time, primarily originated in Escherichia coli, while the enzymes (e.g. amylase) which increased over time were mainly predicted from Bacteroidaceae. Conclusions: The fecal resistome in dairy calves changes dramatically during nursing demonstrating a progressive reduction of ARGs. Colostrum appeared to seed the vast majority ARGs in dairy calves, and the assembly of bovine resistome during early life appears to be driven by significant dietary transitions.