{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,24]],"date-time":"2026-06-24T17:59:15Z","timestamp":1782323955362,"version":"3.54.5"},"reference-count":54,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2021,1,4]],"date-time":"2021-01-04T00:00:00Z","timestamp":1609718400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"China","award":["2019YFC1606000"],"award-info":[{"award-number":["2019YFC1606000"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Salmonella is a globally distributed zoonotic pathogen. Among them, S. pullorum is a host-specific pathogen that seriously affects the development of the poultry breeding industry in China. It mainly infects chickens and can cause white scabs, and the mortality rate after infection is almost 100%. As antibiotics are widely used in animal feed and other production processes, Salmonella resistance has gradually increased. Therefore, there is an increasing need to develop new technologies to control multi-drug resistant (MDR) pathogens and confirm their actual effectiveness in the target food matrix. Bacteriophage can efficiently and specifically lyse bacteria, and will be a potential bactericide to replace antibiotics. In this study, 34 strains of Salmonella bacteriophages were isolated from environmental resources. Therein, phage Pu20 with the widest host spectrum had the strongest ability to lyse tested Salmonella strains. Further studies showed that Pu20 had high pH tolerance and heat resistance, short incubation period. Pu20 can effectively inhibit the growth of two strains of MDR Salmonella in liquid egg white and yolk at 4 \u00b0C and 25 \u00b0C, respectively. According to morphological and phylogenetic analysis, Pu20 belongs to the Podoviridae family. Genomic analysis of Pu20 indicates a linear 59435 bp dsDNA sequence with no homology to virulence or antibiotic resistance-related genes. Together, these results sheds light on the potential biocontrol application value of Pu20 in food products.<\/jats:p>","DOI":"10.3390\/pathogens10010034","type":"journal-article","created":{"date-parts":[[2021,1,4]],"date-time":"2021-01-04T21:58:36Z","timestamp":1609797516000},"page":"34","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":40,"title":["Application of a Novel Lytic Podoviridae Phage Pu20 for Biological Control of Drug-Resistant Salmonella in Liquid Eggs"],"prefix":"10.3390","volume":"10","author":[{"given":"Yu","family":"Zhang","sequence":"first","affiliation":[{"name":"Key Laboratory of Environment Correlative Dietology, Huazhong Agricultural University, Wuhan 430070, China"},{"name":"College of Food Science and Technology, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yifeng","family":"Ding","sequence":"additional","affiliation":[{"name":"Key Laboratory of Environment Correlative Dietology, Huazhong Agricultural University, Wuhan 430070, China"},{"name":"College of Food Science and Technology, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wanning","family":"Li","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenjuan","family":"Zhu","sequence":"additional","affiliation":[{"name":"College of Food Science and Technology, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Environment Correlative Dietology, Huazhong Agricultural University, Wuhan 430070, China"},{"name":"College of Food Science and Technology, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohong","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Environment Correlative Dietology, Huazhong Agricultural University, Wuhan 430070, China"},{"name":"College of Food Science and Technology, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1038\/nrmicro1788","article-title":"Salmonellae Interplay with Host Cells","volume":"6","author":"Haraga","year":"2008","journal-title":"Nat. Rev. Genet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/0167-5877(92)90072-N","article-title":"Village Chickens as a Reservoir of Salmonella pullorum and Salmonella gallinarum in Morocco","volume":"12","author":"Bouzoubaa","year":"1992","journal-title":"Prev. Veter. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1016\/j.foodres.2011.03.057","article-title":"Salmonella and Broiler Processing in the United States: RelationShip to Foodborne Salmonellosis","volume":"45","author":"Finstad","year":"2012","journal-title":"Food Res. Int."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.15585\/mmwr.ss6710a1","article-title":"Surveillance for Foodborne Disease Outbreaks\u2014United States, 2009\u20132015","volume":"67","author":"Manikonda","year":"2018","journal-title":"MMWR. Surveill. Summ."},{"key":"ref_5","unstructured":"CDC (2014). Foodborne Diseases Active Surveillance Network (FoodNet): FoodNet Surveillance Report for 2012 (Final Report)."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2775","DOI":"10.1111\/j.1462-2920.2009.01970.x","article-title":"Position Paper: The Creation of a Rational Scheme for the Nomenclature of Viruses Of Bacteria and Archaea","volume":"11","author":"Kropinski","year":"2009","journal-title":"Environ. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1111\/j.1574-695X.2007.00305.x","article-title":"Analysis of Bacterial Foodborne Disease Outbreaks in China between 1994 and 2005","volume":"51","author":"Wang","year":"2007","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1128\/JCM.42.1.73-78.2004","article-title":"Adaptive Resistance to Biocides in Salmonella enterica and Escherichia coli O157 and Cross-Resistance to Antimicrobial Agents","volume":"42","author":"Braoudaki","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1111\/j.1574-6968.2004.tb09603.x","article-title":"Low Level of Cross-Resistance between Triclosan and Antibiotics in Escherichia coli K-12 and E. coli O55 Compared to E. coli O157","volume":"235","author":"Braoudaki","year":"2004","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"D566","DOI":"10.1093\/nar\/gkw1004","article-title":"CARD 2017: Expansion and Model-Centric Curation of the Comprehensive Antibiotic Resistance Database","volume":"45","author":"Jia","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"108560","DOI":"10.1016\/j.foodres.2019.108560","article-title":"Population Heterogeneity Tactics as Driving Force in Salmonella Virulence and Survival","volume":"125","author":"Staes","year":"2019","journal-title":"Food Res. Int."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Nair, D.V.T., Venkitanarayanan, K., and Johny, A.K. (2018). Antibiotic-Resistant Salmonella in the Food Supply and the Potential Role of Antibiotic Alternatives for Control. Foods, 7.","DOI":"10.3390\/foods7100167"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1016\/j.foodres.2011.04.052","article-title":"Control of Salmonella in Foods by Using Essential Oils: A Review","volume":"45","author":"Bajpai","year":"2012","journal-title":"Food Res. Int."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1146\/annurev-food-030713-092415","article-title":"Phage Therapy in the Food Industry","volume":"5","author":"Endersen","year":"2014","journal-title":"Annu. Rev. Food Sci. Technol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"130","DOI":"10.4161\/bact.1.3.17629","article-title":"Phage-Based Biocontrol Strategies to Reduce Foodborne Pathogens in Foods","volume":"1","author":"Goodridge","year":"2011","journal-title":"Bacteriophage"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.tim.2005.04.003","article-title":"Here a Virus, There a Virus, Everywhere the Same Virus?","volume":"13","author":"Breitbart","year":"2005","journal-title":"Trends Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1016\/j.meegid.2009.05.017","article-title":"Stress-Induced Prophage DNA Replication in Salmonella enterica Serovar Typhimurium","volume":"9","author":"Elrod","year":"2009","journal-title":"Infect. Genet. Evol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1016\/j.tibtech.2010.08.001","article-title":"Bacteriophages as Potential New Therapeutics to Replace or Supplement Antibiotics","volume":"28","author":"Kutateladze","year":"2010","journal-title":"Trends Biotechnol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2874","DOI":"10.1128\/AAC.49.7.2874-2878.2005","article-title":"Human Volunteers Receiving Escherichia coli Phage T4 Orally: A Safety Test of Phage Therapy","volume":"49","author":"Bruttin","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1089\/cmb.2008.0226","article-title":"Estimation of Gene Induction Enables a Relevance-Based Ranking of Gene Sets","volume":"16","author":"Kreutz","year":"2009","journal-title":"J. Comput. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.ijfoodmicro.2019.01.003","article-title":"Control of Salmonella Newport on Cherry Tomato Using a Cocktail of Lytic Bacteriophages","volume":"293","author":"Cucic","year":"2019","journal-title":"Int. J. Food Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.virusres.2017.05.001","article-title":"Characterization of a Broad Host-Spectrum Virulent Salmonella Bacteriophage Fmb-p1 and Its Application on Duck Meat","volume":"236","author":"Wang","year":"2017","journal-title":"Virus Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1046","DOI":"10.3389\/fmicb.2018.01046","article-title":"Isolation, Characterization, and Application of Bacteriophage LPSE1 Against Salmonella enterica in Ready to Eat (RTE) Foods","volume":"9","author":"Huang","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.ijfoodmicro.2011.12.023","article-title":"Biocontrol of Salmonella Typhimurium in RTE Foods with the Virulent Bacteriophage FO1-E2","volume":"154","author":"Guenther","year":"2012","journal-title":"Int. J. Food Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Islam, S., Zhou, Y., Liang, L., Nime, I., Liu, K., Yan, T., Wang, X., and Li, J. (2019). Application of a Phage Cocktail for Control of Salmonella in Foods and Reducing Biofilms. Viruses, 11.","DOI":"10.3390\/v11090841"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3375","DOI":"10.3382\/ps\/pex108","article-title":"Evaluation of the Alpha-Amylase Activity as an Indicator of Pasteurization Efficiency and Microbiological Quality of Liquid Whole Eggs","volume":"96","author":"Menezes","year":"2017","journal-title":"Poult. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"358","DOI":"10.3389\/fmicb.2013.00358","article-title":"Exploring the Risks of Phage Application in the Environment","volume":"4","author":"Meaden","year":"2013","journal-title":"Front. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1111\/j.1574-6968.2006.00217.x","article-title":"Isolation and Characterization of Bacteriophages Infecting Salmonella SPP","volume":"258","author":"Billington","year":"2006","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1128\/AEM.71.3.1387-1393.2005","article-title":"Isolation and Characterization of Novel Giant Stenotrophomonas Maltophilia Phage \u03c6SMA5","volume":"71","author":"Chang","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1007\/978-1-60327-565-1_13","article-title":"Purification of Bacteriophages and SDS-PAGE Analysis of Phage Structural Proteins from Ghost Particles","volume":"502","author":"Boulanger","year":"2009","journal-title":"Methods Mol. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1159\/000150353","article-title":"Taxonomical Classification of 20 Newly Isolated Listeria Bacteriophages by Electron Microscopy and Protein Analysis","volume":"37","author":"Loessner","year":"1994","journal-title":"Intervirology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.1139\/w11-099","article-title":"Characterization of Bacteriophages with a Lytic Effect on Various Salmonella Serotypes and Escherichia Coli O157:H7","volume":"57","author":"Campo","year":"2011","journal-title":"Can. J. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1007\/BF02030117","article-title":"Selection for Bacteriophage Latent Period Length by Bacterial Density: A Theoretical Examination","volume":"18","author":"Abedon","year":"1989","journal-title":"Microb. Ecol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"10200","DOI":"10.1128\/JVI.00865-10","article-title":"Inhibition of Superinfection and the Evolution of Viral Latency","volume":"84","author":"Berngruber","year":"2010","journal-title":"J. Virol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1016\/j.foodres.2018.05.071","article-title":"Isolation, Characterization, and Application of a Novel Specific Salmonella Bacteriophage in Different Food Matrices","volume":"111","author":"Huang","year":"2018","journal-title":"Food Res. Int."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1089\/fpd.2016.2172","article-title":"Treatment of Salmonella-Contaminated Eggs and Pork with a Broad-Spectrum, Single Bacteriophage: Assessment of Efficacy and Resistance Development","volume":"13","author":"Hong","year":"2016","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0092-8674(01)00637-7","article-title":"Phage Genomics","volume":"108","author":"Hendrix","year":"2002","journal-title":"Cell"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1038\/ng0393-266","article-title":"Identification of Protein Coding Regions by Database Similarity Search","volume":"3","author":"Gish","year":"1993","journal-title":"Nat. Genet."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"115D","DOI":"10.1093\/nar\/gkh131","article-title":"UniProt: The Universal Protein Knowledgebase","volume":"32","author":"Apweiler","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2164-9-75","article-title":"The RAST Server: Rapid Annotations using Subsystems Technology","volume":"9","author":"Aziz","year":"2008","journal-title":"BMC Genom."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"W54","DOI":"10.1093\/nar\/gkw413","article-title":"tRNAscan-SE On-line: Integrating search and context for analysis of transfer RNA genes","volume":"44","author":"Lowe","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"D687","DOI":"10.1093\/nar\/gky1080","article-title":"VFDB 2019: A Comparative Pathogenomic Platform with an Interactive Web Interface","volume":"47","author":"Liu","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"W181","DOI":"10.1093\/nar\/gkn179","article-title":"The CGView Server: A Comparative Genomics Tool for Circular Genomes","volume":"36","author":"Grant","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1016\/j.resmic.2008.03.005","article-title":"Unifying Classical and Molecular Taxonomic Classification: Analysis of the Podoviridae Using BLASTP-Based Tools","volume":"159","author":"Lavigne","year":"2008","journal-title":"Res. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Dereeper, A., Audic, S., Claverie, J.-M., and Blanc, G. (2010). BLAST-EXPLORER Helps You Building Datasets for Phylogenetic Analysis. BMC Evol. Biol., 10.","DOI":"10.1186\/1471-2148-10-8"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis Across Computing Platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1804","DOI":"10.3390\/v7041804","article-title":"A Suggested New Bacteriophage Genus, \u201cKp34likevirus\u201d, within the Autographivirinae Subfamily of Podoviridae","volume":"7","author":"Eriksson","year":"2015","journal-title":"Viruses"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1080\/08997659.2016.1249578","article-title":"Isolation and Characterization of Large Marine Bacteriophage (Myoviridae), VhKM4 InfectingVibrio harveyi","volume":"29","author":"Lal","year":"2017","journal-title":"J. Aquat. Anim. Heal."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"109034","DOI":"10.1016\/j.lwt.2020.109034","article-title":"Characterization of a novel T7-like Salmonella Typhimurium (ATCC13311) Bacteriophage LPST144 and its Endolysin","volume":"123","author":"Yang","year":"2020","journal-title":"LWT"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1007\/s12250-014-3523-x","article-title":"Isolation and Characterization of a Lytic Bacteriophage \u03c6Kp-lyy15 of Klebsiella Pneumoniae","volume":"30","author":"Lu","year":"2015","journal-title":"Virol. Sin."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"4836","DOI":"10.3390\/v7082847","article-title":"Bio-Control of Salmonella Enteritidis in Foods Using Bacteriophages","volume":"7","author":"Bao","year":"2015","journal-title":"Viruses"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"109011","DOI":"10.1016\/j.foodres.2020.109011","article-title":"A Broad-Spectrum Phage Controls Multidrug-Resistant Salmonella in Liquid Eggs","volume":"132","author":"Li","year":"2020","journal-title":"Food Res. Int."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"8421","DOI":"10.1021\/jf050964f","article-title":"Advances in the Value of Eggs and Egg Components for Human Health","volume":"53","author":"Phillips","year":"2005","journal-title":"J. Agric. Food Chem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12864-016-3018-2","article-title":"Software-Based Analysis of Bacteriophage Genomes, Physical Ends, and Packaging Strategies","volume":"17","author":"Merrill","year":"2016","journal-title":"BMC Genom."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/1\/34\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:06:53Z","timestamp":1760159213000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/1\/34"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,4]]},"references-count":54,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1]]}},"alternative-id":["pathogens10010034"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10010034","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,4]]}}}