Metagenomic characterization of the microbiome and resistome of retail ground beef products

Authors: DOSTER, ENRIQUE - Texas A&M University; THOMAS, KEVIN - Colorado State University; Weinroth, Margaret - Maggie; PARKER, JENNIFER - Colorado State University; CRONE, KATHRYN - Colorado State University; Arthur, Terrance; Schmidt, John; Wheeler, Tommy; BELK, KEITH - Colorado State University; MORLEY, PAUL - Texas A&M University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/19/2020
Publication Date: 11/6/2020
Citation: Doster, E., Thomas, K.M., Weinroth, M.D., Parker, J.K., Crone, K.K., Arthur, T.M., Schmidt, J.W., Wheeler, T.L., Belk, K.E., Morley, P.S. 2020. Metagenomic characterization of the microbiome and resistome of retail ground beef products. Frontiers in Microbiology. 11. Article 541972.. https://doi.org/10.3389/fmicb.2020.541972.
DOI: https://doi.org/10.3389/fmicb.2020.541972

Interpretive Summary: Ground beef can be a reservoir for a variety of bacteria, including spoilage organisms and pathogenic foodborne bacteria that can exhibit antimicrobial resistance (AMR), which is a public health concern if resistance in pathogens leads to treatment failure in humans. Often, studies of AMR in ground beef employ aerobic culture to isolate marker organisms, but metagenomic sequencing now allows a holistic perspective of the microbial community (microbiome) and the profile of AMR genes they carry (resistome). To date, our study is the first to employ metagenomic sequencing to characterize the resistome of retail ground beef products. Our results suggest that the resistome and microbiome of retail ground beef products with raised without antibiotics (RWA) label claims do not differ from products that do not carry claims regarding antimicrobial drug exposures during cattle production (CONV). This research adds to the growing body of literature suggesting that AMD use in livestock production does not have a strong impact on AMR of bacteria found on food products and highlights the utility of using metagenomic sequencing for future investigations.

Technical Abstract: Ground beef can be a reservoir for a variety of bacteria, including spoilage organisms and pathogenic foodborne bacteria. These bacteria can exhibit antimicrobial resistance (AMR) which is a public health concern if resistance in pathogens leads to treatment failure in humans. Aerobic culture is commonly used to study individual bacterial species, but it is unable to describe the community of microbial species (microbiome) and the profile of AMR genes they carry (resistome), which is critical for getting a holistic perspective of AMR. The objective of this study was to characterize the microbiome and resistome of retail ground beef products labeled as coming from conventional or raised without antibiotics (RWA) production systems. Sixteen ground beef products were purchased from 6 retail grocery outlets in Fort Collins, CO, half of which were labeled as produced from cattle raised conventionally and half of the products were from RWA production. Total DNA was extracted and isolated from each sample and subjected to 16S rRNA amplicon sequencing for microbiome characterization and target-enriched shotgun sequencing to characterize the resistome. Differences in the microbiome and resistome of RWA and conventional ground beef were analyzed using the R programming software. Our results suggest that the resistome and microbiome of retail ground beef products with RWA packaging labels do not differ from products that do not carry claims regarding antimicrobial drug exposures during cattle production. The resistome predominantly consisted of tetracycline resistance making up more than 90% of reads mapped to resistance gene accessions in our samples. Firmicutes and proteobacteria predominated in the microbiome of all samples (65% and 30.2%, respectively), but proteobacteria composed a higher proportion in ground beef from conventionally raised cattle. In addition, our results suggest that product management, such as packaging type, could exert a stronger influence on the microbiome than the resistome in consumer-ready products. Metagenomic analyses of ground beef is a promising tool to investigate community-wide shifts in retail ground beef. Importantly, however, results from metagenomic sequencing must be carefully considered in parallel with traditional methods to better characterize the risk of AMR in retail products.