{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T21:17:35Z","timestamp":1792790255078,"version":"4.5.0"},"reference-count":60,"publisher":"Korean Society of Animal Science and Technology","issue":"4","license":[{"start":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T00:00:00Z","timestamp":1782864000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0"}],"funder":[{"name":"National Research Foundation of Korea","award":["RS-2025-16068814"],"award-info":[{"award-number":["RS-2025-16068814"]}],"id":[{"id":"https:\/\/ror.org\/013aysd81","id-type":"ROR","asserted-by":"crossref"}]},{"name":"National Research Foundation of Korea","award":["RS-2023-00218476"],"award-info":[{"award-number":["RS-2023-00218476"]}],"id":[{"id":"https:\/\/ror.org\/013aysd81","id-type":"ROR","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.ejast.org"],"crossmark-restriction":true},"short-container-title":["J Anim Sci Technol"],"published-print":{"date-parts":[[2026,7]]},"abstract":"<jats:p>Salmonella is a critical foodborne pathogen that significantly\n                    affects global food safety and the poultry industry. The reliance on antibiotics\n                    to control Salmonella infections has led to the emergence of\n                    antibiotic-resistant bacteria, necessitating the development of alternative\n                    strategies. The present study explored the synergistic potential of combining\n                    bacteriophages and probiotics as a dual approach for Salmonella\n                    suppression and gut microbiota modulation. Using a multi-omics approach\n                    integrating culture and metagenomics, we isolated Lactobacillus\n                    reuteri J2M1, a robust probiotic strain with strong acid and\n                    bile tolerance, intestinal adhesion, and a safety profile. Concurrently, two\n                    bacteriophages, SLAM_phiST45 and SLAM_phiST56, targeting\n                        Salmonella Typhimurium were selected based on their broad\n                    host range, enhanced inhibitory effects as a cocktail, and genomic safety\n                    validated through whole-genome sequencing. In a model that simulated the gut\n                    environment of poultry, the combined application of bacteriophages and\n                        L. reuteri J2M1 resulted in significant changes in the\n                    microbial community at the genus level. Although the application of\n                    bacteriophages alone effectively reduced Salmonella\n                    populations, it also led to the proliferation of genera that contain potential\n                    pathogens, such as Clostridium perfringens. In contrast, the\n                    co-application of L. reuteri J2M1 mitigated these negative\n                    effects by promoting the growth of beneficial genera, including\n                        Oscillibacter and Clostridium butyricum,\n                    which are associated with anti-inflammatory properties and gut health. These\n                    findings demonstrate that combining bacteriophages with probiotics suppresses\n                    pathogens as well as contributes to the establishment of a balanced gut\n                    microbial community. This study highlights the utility of a multi-omics approach\n                    for probiotic discovery, the efficacy of bacteriophage cocktails in pathogen\n                    suppression, and the benefits of their synergistic application with probiotics.\n                    Although in vivo validation is required, these in\n                        vitro results provide a robust foundation for the development of\n                    sustainable and effective alternatives to antibiotics for poultry\n                    production.<\/jats:p>","DOI":"10.5187\/jast.2025.e30","type":"journal-article","created":{"date-parts":[[2025,4,14]],"date-time":"2025-04-14T04:18:12Z","timestamp":1744604292000},"page":"1213-1238","update-policy":"https:\/\/doi.org\/10.5187\/crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Exploring synergistic effect of bacteriophages with probiotics\n                    against multidrug resistant Salmonella Typhimurium in a\n                    simulated chicken gastrointestinal system using metagenomic- and culturomic\n                    approaches"],"prefix":"10.5187","volume":"68","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9444-3237","authenticated-orcid":false,"given":"Youbin","family":"Choi","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04h9pn542","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Science, Seoul National University, Seoul, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0208-6234","authenticated-orcid":false,"given":"Anna","family":"Kang","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04h9pn542","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Science, Seoul National University, Seoul, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2204-6443","authenticated-orcid":false,"given":"Min-Geun","family":"Kang","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04h9pn542","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Science, Seoul National University, Seoul, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7224-3958","authenticated-orcid":false,"given":"Daniel Junpyo","family":"Lee","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04h9pn542","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Science, Seoul National University, Seoul, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-1065-9743","authenticated-orcid":false,"given":"Dawon","family":"Kyoung","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04h9pn542","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Science, Seoul National University, Seoul, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3693-1320","authenticated-orcid":false,"given":"Jung Min","family":"Heo","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0227as991","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Animal Science and Biotechnology, Chungnam National University, Daejeon, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4515-5212","authenticated-orcid":false,"given":"Minho","family":"Song","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0227as991","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Animal Science and Biotechnology, Chungnam National University, Daejeon, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2428-412X","authenticated-orcid":false,"given":"Sangnam","family":"Oh","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/015v9d997","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Functional Food and Biotechnology, Jeonju University, Jeonju, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6769-0657","authenticated-orcid":false,"given":"Younghoon","family":"Kim","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04h9pn542","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Science, Seoul National University, Seoul, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"3132","published-online":{"date-parts":[[2026,7,31]]},"reference":[{"key":"key2.0261002113954e+13_B1","doi-asserted-by":"crossref","first-page":"106","DOI":"10.5187\/jast.2023.e119","article-title":"Effects of probiotics on growth performance, intestinal\n                        morphology, intestinal microbiota weaning pig challenged with Escherichia\n                        coli and Salmonella enterica","volume":"67","author":"Song","year":"2025","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B2","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.5187\/jast.2024.e9","article-title":"Complete genome of blaCTX-M-65-carrying Salmonella infantis\n                        strain Z01323CSL0015 isolated from broiler chicken","volume":"67","author":"Oh","year":"2024","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B3","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.5187\/jast.2024.e71","article-title":"Supplemental illite or in combination with probiotics improves\n                        performance and gut health in broilers challenged with Salmonella\n                        typhimurium","volume":"67","author":"Kim","year":"2024","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B4","doi-asserted-by":"crossref","first-page":"266","DOI":"10.5187\/jast.2023.e129","article-title":"Antibiotic resistance in livestock, environment and humans: one\n                        health perspective","volume":"66","author":"Pandey","year":"2024","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B5","doi-asserted-by":"crossref","first-page":"872","DOI":"10.3390\/ani10050872","article-title":"The use of bacteriophages in the poultry industry","volume":"10","author":"bikowska","year":"2020","journal-title":"Animals."},{"key":"key2.0261002113954e+13_B6","doi-asserted-by":"crossref","first-page":"6600","DOI":"10.1128\/AEM.01257-12","article-title":"Significance of the bacteriophage treatment schedule in reducing\n                        Salmonella colonization of poultry","volume":"78","author":"Bardina","year":"2012","journal-title":"Appl Environ Microbiol."},{"key":"key2.0261002113954e+13_B7","doi-asserted-by":"crossref","first-page":"232","DOI":"10.5187\/jast.2023.e40","article-title":"Complete genome sequence of bacteriocin-producing\n                        Ligilactobacillus salivarius B4311 isolated from fecal samples of broiler\n                        chicken with anti-listeria activity","volume":"66","author":"Han","year":"2024","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B8","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.5187\/jast.2024.e50","article-title":"Complete genome sequence of potential probiotic Ligilactobacillus\n                        ruminis CACC881 isolated from swine","volume":"67","author":"Park","year":"2025","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B9","doi-asserted-by":"crossref","first-page":"489","DOI":"10.5187\/jast.2024.e29","article-title":"Complete genome sequence of Ligilactobacillus agilis LDTM47,\n                        bacteriocin-producing lactic acid bacteria isolated from broiler\n                        gastrointestinal tract","volume":"67","author":"Eum","year":"2025","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B10","doi-asserted-by":"crossref","first-page":"887799","DOI":"10.3389\/fmicb.2022.887799","article-title":"Bacteriophage cocktail and microcin-producing probiotic\n                        Escherichia coli protect mice against gut colonization with\n                        multidrug-resistant Escherichia coli sequence type 131","volume":"13","author":"Porter","year":"2022","journal-title":"Front Microbiol."},{"key":"key2.0261002113954e+13_B11","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.3390\/ani13081328","article-title":"Effects of phage cocktail, probiotics, and their combination on\n                        growth performance and gut microbiota of broiler chickens","volume":"13","author":"Shaufi","year":"2023","journal-title":"Animals."},{"key":"key2.0261002113954e+13_B12","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1128\/AAC.45.3.649-659.2001","article-title":"Bacteriophage therapy","volume":"45","author":"Sulakvelidze","year":"2001","journal-title":"Antimicrob Agents Chemother."},{"key":"key2.0261002113954e+13_B13","doi-asserted-by":"crossref","first-page":"449","DOI":"10.2146\/ajhp090168","article-title":"Probiotics","volume":"67","author":"Williams","year":"2010","journal-title":"Am J Health Syst Pharm."},{"key":"key2.0261002113954e+13_B14","doi-asserted-by":"crossref","first-page":"skac323","DOI":"10.1093\/jas\/skac323","article-title":"Culturomic-, metagenomic-, and transcriptomic-based\n                        characterization of commensal lactic acid bacteria isolated from domestic\n                        dogs using Caenorhabditis elegans as a model for aging","volume":"100","author":"Kang","year":"2022","journal-title":"J Anim Sci."},{"key":"key2.0261002113954e+13_B15","doi-asserted-by":"crossref","first-page":"1314","DOI":"10.5187\/jast.2021.e109","article-title":"Effects of Bacillus-based probiotics on growth performance,\n                      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sources, species, and\n                        dynamics","volume":"5","author":"Rouger","year":"2017","journal-title":"Microorganisms."},{"key":"key2.0261002113954e+13_B19","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1186\/s42523-022-00212-w","article-title":"Molecular characterization of gut microbiome in weaning pigs\n                        supplemented with multi-strain probiotics using metagenomic, culturomic, and\n                        metabolomic approaches","volume":"4","author":"Lee","year":"2022","journal-title":"Anim Microbiome."},{"key":"key2.0261002113954e+13_B20","first-page":"1","article-title":"Kirby-Bauer disk diffusion susceptibility test\n                        protocol","volume":"15","author":"Hudzicki","year":"2009","journal-title":"Am Socr Microbiol."},{"key":"key2.0261002113954e+13_B21","first-page":"1152","article-title":"Measuring Caenorhabditis elegans life span on solid\n                        media","author":"Sutphin","year":"2009","journal-title":"J Vis Exp."},{"key":"key2.0261002113954e+13_B22","doi-asserted-by":"crossref","first-page":"4070","DOI":"10.1128\/AEM.00428-08","article-title":"Isolation and characterization of bacteriophages infecting the\n                        fish pathogen flavobacterium psychrophilum","volume":"74","author":"Stenholm","year":"2008","journal-title":"Appl Environ Microbiol."},{"key":"key2.0261002113954e+13_B23","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0118557","article-title":"Isolation of phages for phage therapy: a comparison of spot tests\n                        and efficiency of plating analyses for determination of host range and\n                        efficacy","volume":"10","author":"Khan Mirzaei","year":"2015","journal-title":"PLOS ONE."},{"key":"key2.0261002113954e+13_B24","doi-asserted-by":"crossref","first-page":"3523","DOI":"10.1007\/s00705-017-3513-z","article-title":"Virus purification by CsCl density gradient using general\n                        centrifugation","volume":"162","author":"Nasukawa","year":"2017","journal-title":"Arch Virol."},{"key":"key2.0261002113954e+13_B25","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.fm.2012.02.003","article-title":"Bacteriophages BCP1-1 and BCP8-2 require divalent cations for\n                        efficient control of Bacillus cereus in fermented foods","volume":"31","author":"Bandara","year":"2012","journal-title":"Food Microbiol."},{"key":"key2.0261002113954e+13_B26","doi-asserted-by":"crossref","first-page":"240","DOI":"10.3390\/v10050240","article-title":"Complete nucleotide sequence analysis of a novel Bacillus\n                        subtilis-infecting bacteriophage BSP10 and its effect on poly-gamma-glutamic\n                        acid degradation","volume":"10","author":"Ghosh","year":"2018","journal-title":"Viruses."},{"key":"key2.0261002113954e+13_B27","doi-asserted-by":"crossref","first-page":"865","DOI":"10.3390\/v13050865","article-title":"Evaluation of the stability of bacteriophages in different\n                        solutions suitable for the production of magistral preparations in\n                        Belgium","volume":"13","author":"Duyvejonck","year":"2021","journal-title":"Viruses."},{"key":"key2.0261002113954e+13_B28","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1038\/s41587-019-0072-8","article-title":"Assembly of long, error-prone reads using repeat\n                        graphs","volume":"37","author":"Kolmogorov","year":"2019","journal-title":"Nat Biotechnol."},{"key":"key2.0261002113954e+13_B29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2164-9-75","article-title":"The RAST server: rapid annotations using subsystems\n                        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on\n                        Taxonomy of Viruses (ICTV)","volume":"46","author":"Lefkowitz","year":"2018","journal-title":"Nucleic Aacids Res."},{"key":"key2.0261002113954e+13_B36","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1007\/s10482-017-0844-4","article-title":"A large-scale evaluation of algorithms to calculate average\n                        nucleotide identity","volume":"110","author":"Yoon","year":"2017","journal-title":"Antonie van Leeuwenhoek."},{"key":"key2.0261002113954e+13_B37","first-page":"10.3.1","article-title":"Using MUMmer to identify similar regions in large sequence\n                        sets","author":"Delcher","year":"2003","journal-title":"Curr Protoc Bioinform."},{"key":"key2.0261002113954e+13_B38","doi-asserted-by":"crossref","first-page":"1100","DOI":"10.1099\/ijsem.0.000760","article-title":"OrthoANI: an improved algorithm and software for calculating\n                        average nucleotide identity","volume":"66","author":"Lee","year":"2016","journal-title":"Int J Syst Evol Microbiol."},{"key":"key2.0261002113954e+13_B39","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1016\/j.resmic.2011.07.001","article-title":"Prevalence of Bacillus cereus bacteriophages in fermented foods\n                        and characterization of phage JBP901","volume":"162","author":"Shin","year":"2011","journal-title":"Res Microbiol."},{"key":"key2.0261002113954e+13_B40","doi-asserted-by":"crossref","first-page":"uqae003","DOI":"10.1093\/femsml\/uqae003","article-title":"Multireceptor phage cocktail against Salmonella enterica to\n                        circumvent phage resistance","volume":"5","author":"Martinez-Soto","year":"2024","journal-title":"microLife"},{"key":"key2.0261002113954e+13_B41","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1007\/978-1-60327-164-6_14","article-title":"Phage host range and efficiency of plating","volume-title":"Bacteriophages. Methods and protocols","author":"Kutter","year":"2009"},{"key":"key2.0261002113954e+13_B42","doi-asserted-by":"crossref","first-page":"968","DOI":"10.3390\/applmicrobiol3030066","article-title":"Development of a chicken gastrointestinal tract (GIT) simulation\n                        model: impact of cecal inoculum storage preservation\n                        conditions","volume":"3","author":"de Carvalho","year":"2023","journal-title":"Appl Microbiol."},{"key":"key2.0261002113954e+13_B43","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/s42523-024-00303-w","article-title":"Dietary L-methionine modulates the gut microbiota and improves\n                        the expression of tight junctions in an in vitro model of the chicken\n                        gastrointestinal tract","volume":"6","author":"Kwak","year":"2024","journal-title":"Anim Microbiome."},{"key":"key2.0261002113954e+13_B44","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0206316","article-title":"Rapid detection and differentiation of Salmonella species,\n                        Salmonella typhimurium and Salmonella enteritidis by multiplex quantitative\n                        PCR","volume":"13","author":"Heymans","year":"2018","journal-title":"PLOS ONE."},{"key":"key2.0261002113954e+13_B45","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1186\/s12866-021-02233-y","article-title":"Optimisation of sample storage and DNA extraction for human gut\n                        microbiota studies","volume":"21","author":"Kazantseva","year":"2021","journal-title":"BMC Microbiol."},{"key":"key2.0261002113954e+13_B46","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1186\/s12864-023-09623-8","article-title":"Assessment of beneficial effects and identification of host\n                        adaptation-associated genes of Ligilactobacillus salivarius isolated from\n                        badgers","volume":"24","author":"Wang","year":"2023","journal-title":"BMC Genomics."},{"key":"key2.0261002113954e+13_B47","doi-asserted-by":"crossref","first-page":"1411482","DOI":"10.3389\/fcimb.2024.1411482","article-title":"Research progress in isolation and identification of rumen\n                        probiotics","volume":"14","author":"Wu","year":"2024","journal-title":"Front Cell Infect Microb."},{"key":"key2.0261002113954e+13_B48","doi-asserted-by":"crossref","first-page":"3045","DOI":"10.3390\/ijms24033045","article-title":"Culturing the chicken intestinal microbiota and potential\n                        application as probiotics development","volume":"24","author":"Ma","year":"2023","journal-title":"Int J Mol Sci."},{"key":"key2.0261002113954e+13_B49","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1038\/nature17645","article-title":"Culturing of \u2018unculturable\u2019 human microbiota\n                        reveals novel taxa and extensive sporulation","volume":"533","author":"Browne","year":"2016","journal-title":"Nature."},{"key":"key2.0261002113954e+13_B50","doi-asserted-by":"crossref","first-page":"57","DOI":"10.5187\/jast.2024.e5","article-title":"The current state of phage therapy in livestock and companion\n                        animals","volume":"66","author":"Choi","year":"2024","journal-title":"J Anim Sci Technol."},{"key":"key2.0261002113954e+13_B51","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.fm.2018.08.011","article-title":"Effective inhibition of Salmonella typhimurium in fresh produce\n                        by a phage cocktail targeting multiple host receptors","volume":"77","author":"Bai","year":"2019","journal-title":"Food Microbiol."},{"key":"key2.0261002113954e+13_B52","first-page":"e01462","article-title":"Phage-antibiotic synergy is driven by a unique combination of\n                        antibacterial mechanism of action and 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