{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,8]],"date-time":"2026-03-08T09:52:37Z","timestamp":1772963557632,"version":"3.50.1"},"reference-count":30,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,7,13]],"date-time":"2023-07-13T00:00:00Z","timestamp":1689206400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Metagenomics analysis of foods has the potential to provide comprehensive data on the presence and prevalence of antimicrobial resistance (AMR) genes in the microbiome of foods. However, AMR genes are generally present in low abundance compared to other bacterial genes in the food microbiome and consequently require multiple rounds of in-depth sequencing for detection. Here, a metagenomics approach, using bait-capture probes targeting antimicrobial resistance and plasmid genes, is used to characterize the resistome and plasmidome of retail beef, chicken, oyster, shrimp, and veal enrichment cultures (<jats:italic>n<\/jats:italic>\u2009=\u200915). Compared to total shotgun metagenomics, bait-capture required approximately 40-fold fewer sequence reads to detect twice the number of AMR gene classes, AMR gene families, and plasmid genes across all sample types. For the detection of critically important extended spectrum beta-lactamase (ESBL) genes the bait capture method had a higher overall positivity rate (44%) compared to shotgun metagenomics (26%), and a culture-based method (29%). Overall, the results support the use of bait-capture for the identification of low abundance genes such as AMR genes from food samples.<\/jats:p>","DOI":"10.3389\/fmicb.2023.1188872","type":"journal-article","created":{"date-parts":[[2023,7,13]],"date-time":"2023-07-13T18:12:14Z","timestamp":1689271934000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Targeted metagenomics using bait-capture to detect antibiotic resistance genes in retail meat and seafood"],"prefix":"10.3389","volume":"14","author":[{"given":"Annika","family":"Flint","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ashley","family":"Cooper","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mary","family":"Rao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kelly","family":"Weedmark","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Catherine","family":"Carrillo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sandeep","family":"Tamber","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,7,13]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1804","DOI":"10.1128\/jcm.02638-15","article-title":"Use of shotgun metagenome sequencing to detect fecal colonization with multidrug-resistant bacteria in children","volume":"54","author":"Andersen","year":"2016","journal-title":"J. Clin. Microbiol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"6551","DOI":"10.1128\/aac.00933-15","article-title":"The human gut microbiome as a transporter of antibiotic resistance genes between continents","volume":"59","author":"Bengtsson-Palme","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"2690","DOI":"10.1093\/jac\/dkx199","article-title":"Using metagenomics to investigate human and environmental resistomes","volume":"72","author":"Bengtsson-Palme","year":"2017","journal-title":"J. Antimicrob. Chemother."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"3895","DOI":"10.1128\/aac.02412-14","article-title":"In silico detection and typing of plasmids using plasmid finder and plasmid multilocus sequence typing","volume":"58","author":"Carattoli","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"e296","DOI":"10.1017\/s0950268819001778","article-title":"Ceftiofur-resistant Salmonella enterica serovar Heidelberg of poultry origin - a risk profile using the codex framework","volume":"147","author":"Carson","year":"2019","journal-title":"Epidemiol. Infect."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"dlab092","DOI":"10.1093\/jacamr\/dlab092","article-title":"Extended-spectrum \u03b2-lactamases: an update on their characteristics, epidemiology and detection","volume":"3","author":"Castanheira","year":"2021","journal-title":"JAC Antimicrob Resist"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"fastp: an ultra-fast all-in-one FASTQ preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"e0067722","DOI":"10.1128\/aac.00677-22","article-title":"A one health genomic investigation of gentamicin resistance in Escherichia coli from human and chicken sources in Canada, 2014 to 2017","volume":"66","author":"Cox","year":"2022","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1016\/j.ijmm.2013.02.008","article-title":"CTX-M-type \u03b2-lactamases: a successful story of antibiotic resistance","volume":"303","author":"D'Andrea","year":"2013","journal-title":"Int. J. Med. Microbiol."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"giab008","DOI":"10.1093\/gigascience\/giab008","article-title":"Twelve years of SAMtools and BCFtools","volume":"10","author":"Danecek","year":"2021","journal-title":"Gigascience"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"2902","DOI":"10.1111\/jam.15738","article-title":"'To be, or not to be'-the dilemma of 'silent' antimicrobial resistance genes in bacteria","volume":"133","author":"Deekshit","year":"2022","journal-title":"J. Appl. Microbiol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.3389\/fmicb.2017.01069","article-title":"Metagenomics: the next culture-independent game changer","volume":"8","author":"Forbes","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"e01324-19","DOI":"10.1128\/aac.01324-19","article-title":"Capturing the resistome: a targeted capture method to reveal antibiotic resistance determinants in metagenomes","volume":"64","author":"Guitor","year":"2019","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1186\/s13073-014-0090-6","article-title":"SRST2: rapid genomic surveillance for public health and hospital microbiology labs","volume":"6","author":"Inouye","year":"2014","journal-title":"Genome Med."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1186\/s40168-017-0387-y","article-title":"In-depth resistome analysis by targeted metagenomics","volume":"6","author":"Lanza","year":"2018","journal-title":"Microbiome"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1081\/abio-120005771","article-title":"The food safety perspective of antibiotic resistance","volume":"13","author":"McDermott","year":"2002","journal-title":"Anim. Biotechnol."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"e61217","DOI":"10.1371\/journal.pone.0061217","article-title":"Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data","volume":"8","author":"McMurdie","year":"2013","journal-title":"PLoS One"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.ijfoodmicro.2018.02.022","article-title":"Exposure to antimicrobial-resistant Escherichia coli through the consumption of ground beef in Western Canada","volume":"272","author":"Nekouei","year":"2018","journal-title":"Int. J. Food Microbiol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1186\/s40168-017-0361-8","article-title":"Enrichment allows identification of diverse, rare elements in metagenomic resistome-virulome sequencing","volume":"5","author":"Noyes","year":"2017","journal-title":"Microbiome"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.mib.2014.09.002","article-title":"The antibiotic resistome: what's new?","volume":"21","author":"Perry","year":"2014","journal-title":"Curr. Opin. Microbiol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"e0222831","DOI":"10.1371\/journal.pone.0222831","article-title":"Selective culture enrichment and sequencing of feces to enhance detection of antimicrobial resistance genes in third-generation cephalosporin resistant Enterobacteriaceae","volume":"14","author":"Peto","year":"2019","journal-title":"PLoS One"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1136\/vr.105640","article-title":"Trends in Salmonella serovars and antimicrobial resistance in pigs and poultry in Northern Ireland between 1997 and 2016","volume":"186","author":"Porter","year":"2020","journal-title":"Vet. Rec."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"2943","DOI":"10.1093\/bioinformatics\/btac166","article-title":"Analysing high-throughput sequencing data in Python with HTSeq 2.0","volume":"38","author":"Putri","year":"2022","journal-title":"Bioinformatics"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1016\/j.ijfoodmicro.2016.10.036","article-title":"Evaluation of meat, fruit and vegetables from retail stores in five United Kingdom regions as sources of extended-spectrum beta-lactamase (ESBL)-producing and carbapenem-resistant Escherichia coli","volume":"241","author":"Randall","year":"2017","journal-title":"Int. J. Food Microbiol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"106314","DOI":"10.1016\/j.mimet.2021.106314","article-title":"Isolation of third generation cephalosporin resistant Enterobacteriaceae from retail meats and detection of extended spectrum beta-lactamase activity","volume":"189","author":"Rao","year":"2021","journal-title":"J. Microbiol. Methods"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"1749","DOI":"10.4315\/jfp-21-005","article-title":"A national antimicrobial resistance monitoring system survey of antimicrobial-resistant foodborne bacteria isolated from retail veal in the United States","volume":"84","author":"Tate","year":"2021","journal-title":"J. Food Prot."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"203","DOI":"10.3389\/fmicb.2011.00203","article-title":"Acquired antibiotic resistance genes: an overview","volume":"2","author":"van Hoek","year":"2011","journal-title":"Front. Microbiol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"966207","DOI":"10.3389\/fmicb.2022.966207","article-title":"Formic acid, an organic acid food preservative, induces viable-but-non-culturable state, and triggers new antimicrobial resistance traits in Acinetobacter baumannii and Klebsiella pneumoniae","volume":"13","author":"Yadav","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"2640","DOI":"10.1093\/jac\/dks261","article-title":"Identification of acquired antimicrobial resistance genes","volume":"67","author":"Zankari","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1186\/1471-2164-13-703","article-title":"Targeted enrichment of the black cottonwood (Populus trichocarpa) gene space using sequence capture","volume":"13","author":"Zhou","year":"2012","journal-title":"BMC Genomics"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1188872\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,13]],"date-time":"2023-07-13T18:12:18Z","timestamp":1689271938000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1188872\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,13]]},"references-count":30,"alternative-id":["10.3389\/fmicb.2023.1188872"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1188872","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,13]]},"article-number":"1188872"}}