{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T23:58:47Z","timestamp":1790812727157,"version":"4.1.0"},"reference-count":41,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,12,8]],"date-time":"2022-12-08T00:00:00Z","timestamp":1670457600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"ational Key Research and Development Plan","award":["2021YFC1200205"],"award-info":[{"award-number":["2021YFC1200205"]}]},{"name":"ational Key Research and Development Plan","award":["82002197"],"award-info":[{"award-number":["82002197"]}]},{"name":"ational Key Research and Development Plan","award":["2021ZD0006"],"award-info":[{"award-number":["2021ZD0006"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2021YFC1200205"],"award-info":[{"award-number":["2021YFC1200205"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82002197"],"award-info":[{"award-number":["82002197"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2021ZD0006"],"award-info":[{"award-number":["2021ZD0006"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Key Scientific and Technology Project of Inner Mongolia Autonomous Region","award":["2021YFC1200205"],"award-info":[{"award-number":["2021YFC1200205"]}]},{"name":"Key Scientific and Technology Project of Inner Mongolia Autonomous Region","award":["82002197"],"award-info":[{"award-number":["82002197"]}]},{"name":"Key Scientific and Technology Project of Inner Mongolia Autonomous Region","award":["2021ZD0006"],"award-info":[{"award-number":["2021ZD0006"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Bacteriophages (phages) have been successfully used as disinfectors to kill bacteria in food and the environment and have been used medically for curing human diseases. The objective of this research was to elucidate the morphological and genomic characteristics of two novel Yersinia pestis phages, vB_YpeM_ MHS112 (MHS112) and vB_YpeM_GMS130 (GMS130), belonging to the genus Gaprivervirus, subfamily Tevenvirinae, family Myoviridae. Genome sequencing showed that the sizes of MHS112 and GMS130 were 170507 and 168552 bp, respectively. A total of 303 and 292 open reading frames with 2 tRNA and 3 tRNA were predicted in MHS112 and GMS130, respectively. The phylogenetic relationships were analysed among the two novel Y. pestis phages, phages in the genus Gaprivervirus, and several T4-like phages infecting the Yersinia genus. The bacteriophage MHS112 and GMS130 exhibited a wider lytic host spectrum and exhibited comparative temperature and pH stability. Such features signify that these phages do not need to rely on Y. pestis as their host bacteria in the ecological environment, while they could be based on more massive Enterobacteriales species to propagate and form ecological barriers against Y. pestis pathogens colonised in plague foci. Such characteristics indicated that the two phages have potential as biocontrol agents for eliminating the endemics of animal plague in natural plague foci.<\/jats:p>","DOI":"10.3390\/v14122740","type":"journal-article","created":{"date-parts":[[2022,12,9]],"date-time":"2022-12-09T02:50:51Z","timestamp":1670554251000},"page":"2740","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Two Novel Yersinia pestis Bacteriophages with a Broad Host Range: Potential as Biocontrol Agents in Plague Natural Foci"],"prefix":"10.3390","volume":"14","author":[{"given":"Haixiao","family":"Jin","sequence":"first","affiliation":[{"name":"National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China"},{"name":"State Key Laboratory of Infectious Disease Prevention and Control, Beijing 102206, China"},{"name":"Department of Public Health, Medical Institute of Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Youhong","family":"Zhong","sequence":"additional","affiliation":[{"name":"Yunnan Institute for Endemic Disease Control and Prevention, Dali 671000, China"},{"name":"Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Dali 671000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yiting","family":"Wang","sequence":"additional","affiliation":[{"name":"National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China"},{"name":"State Key Laboratory of Infectious Disease Prevention and Control, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chuanyu","family":"Zhang","sequence":"additional","affiliation":[{"name":"National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China"},{"name":"State Key Laboratory of Infectious Disease Prevention and Control, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Guo","sequence":"additional","affiliation":[{"name":"National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China"},{"name":"State Key Laboratory of Infectious Disease Prevention and Control, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaona","family":"Shen","sequence":"additional","affiliation":[{"name":"National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China"},{"name":"State Key Laboratory of Infectious Disease Prevention and Control, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cunxiang","family":"Li","sequence":"additional","affiliation":[{"name":"Qinghai Institute for Endemic Disease Control and Prevention, Xining 811602, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Huang","sequence":"additional","affiliation":[{"name":"National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China"},{"name":"State Key Laboratory of Infectious Disease Prevention and Control, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haoming","family":"Xiong","sequence":"additional","affiliation":[{"name":"Department of Public Health, Medical Institute of Qinghai University, Xining 810016, China"},{"name":"Qinghai Institute for Endemic Disease Control and Prevention, Xining 811602, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peng","family":"Wang","sequence":"additional","affiliation":[{"name":"Yunnan Institute for Endemic Disease Control and Prevention, Dali 671000, China"},{"name":"Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Dali 671000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Li","sequence":"additional","affiliation":[{"name":"National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China"},{"name":"State Key Laboratory of Infectious Disease Prevention and Control, Beijing 102206, China"},{"name":"Department of Public Health, Medical Institute of Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1038\/ng.705","article-title":"Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity","volume":"42","author":"Morelli","year":"2010","journal-title":"Nat. Genet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3201\/eid0701.010106","article-title":"Transferable plasmid-mediated resistance to streptomycin in a clinical isolate of Yersinia pestis","volume":"7","author":"Guiyoule","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1056\/NEJM199709043371004","article-title":"Multidrug resistance in Yersinia pestis mediated by a transferable plasmid","volume":"337","author":"Galimand","year":"1997","journal-title":"N. Engl. J. Med."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Dai, R., He, J., Zha, X., Wang, Y., Zhang, X., Gao, H., Yang, X., Li, J., Xin, Y., and Wang, Y. (2021). A novel mechanism of streptomycin resistance in Yersinia pestis: Mutation in the rpsL gene. PLoS Negl. Trop. Dis., 15.","DOI":"10.1371\/journal.pntd.0009324"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1093\/cid\/ciab606","article-title":"Transmission of Antimicrobial Resistant Yersinia pestis during a Pneumonic Plague Outbreak","volume":"74","author":"Andrianaivoarimanana","year":"2022","journal-title":"Clin. Infect. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"198628","DOI":"10.1016\/j.virusres.2021.198628","article-title":"Characterization and genome analysis of a broad lytic spectrum bacteriophage P479 against multidrug-resistant Escherichia coli","volume":"308","author":"Li","year":"2022","journal-title":"Virus Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1007\/978-94-024-0890-4_13","article-title":"Bacteriophages of Yersinia pestis","volume":"918","author":"Zhao","year":"2016","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Filippov, A.A., Sergueev, K.V., He, Y., Huang, X.Z., Gnade, B.T., Mueller, A.J., Fernandez-Prada, C.M., and Nikolich, M.P. (2011). Bacteriophage-resistant mutants in Yersinia pestis: Identification of phage receptors and attenuation for mice. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0025486"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"12260","DOI":"10.1128\/JVI.01948-13","article-title":"Outer membrane proteins ail and OmpF of Yersinia pestis are involved in the adsorption of T7-related bacteriophage Yep-phi","volume":"87","author":"Zhao","year":"2013","journal-title":"J. Virol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/978-1-4614-3561-7_16","article-title":"Bacteriophages capable of lysing Yersinia pestis and Yersinia pseudotuberculosis: Efficiency of plating tests and identification of receptors in escherichia coli K-12","volume":"954","author":"Filippov","year":"2012","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"168","DOI":"10.4161\/bact.22240","article-title":"A Yersinia pestis-specific, lytic phage preparation significantly reduces viable Y. pestis on various hard surfaces experimentally contaminated with the bacterium","volume":"2","author":"Rashid","year":"2012","journal-title":"Bacteriophage"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"4963","DOI":"10.1128\/JB.00339-11","article-title":"Identification of the lipopolysaccharide core of Yersinia pestis and Yersinia pseudotuberculosis as the receptor for bacteriophage phiA1122","volume":"193","author":"Kiljunen","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1099\/vir.0.026328-0","article-title":"The complete genome sequence and proteomics of Yersinia pestis phage Yep-phi","volume":"92","author":"Zhao","year":"2011","journal-title":"J. Gen. Virol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.virol.2010.07.048","article-title":"Insights into the infective properties of YpfPhi, the Yersinia pestis filamentous phage","volume":"407","author":"Chouikha","year":"2010","journal-title":"Virology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.virol.2007.10.032","article-title":"Molecular characterization of L-413C, a P2-related plague diagnostic bacteriophage","volume":"372","author":"Garcia","year":"2008","journal-title":"Virology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"198934","DOI":"10.1016\/j.virusres.2022.198934","article-title":"Identification and characterization of P2-like bacteriophages of Yersinia pestis","volume":"322","author":"Qi","year":"2022","journal-title":"Virus Res."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Salem, M., Pajunen, M.I., Jun, J.W., and Skurnik, M. (2021). T4-like Bacteriophages Isolated from Pig Stools Infect Yersinia pseudotuberculosis and Yersinia pestis Using LPS and OmpF as Receptors. Viruses, 13.","DOI":"10.3390\/v13020296"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Skurnik, M., Jaakkola, S., Mattinen, L., von Ossowski, L., Nawaz, A., Pajunen, M.I., and Happonen, L.J. (2021). Bacteriophages fEV-1 and fD1 Infect Yersinia pestis. Viruses, 13.","DOI":"10.3390\/v13071384"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"197982","DOI":"10.1016\/j.virusres.2020.197982","article-title":"The characteristics and genome analysis of the novel Y. pestis phage JC221","volume":"283","author":"Yuan","year":"2020","journal-title":"Virus Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1007\/s11262-015-1222-9","article-title":"Isolation and characterization of a bacteriophage with broad host range, displaying potential in preventing bovine diarrhoea","volume":"51","author":"Anand","year":"2015","journal-title":"Virus Genes"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e0222021","DOI":"10.1128\/spectrum.02220-21","article-title":"Characterization of a T4-like Bacteriophage vB_EcoM-Sa45lw as a Potential Biocontrol Agent for Shiga Toxin-Producing Escherichia coli O45 Contaminated on Mung Bean Seeds","volume":"10","author":"Liao","year":"2022","journal-title":"Microbiol. Spectrum"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/2047-217X-1-18","article-title":"SOAPdenovo2: An empirically improved memory-efficient short-read de novo assembler","volume":"1","author":"Luo","year":"2012","journal-title":"Gigascience"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1093\/bioinformatics\/btr039","article-title":"Easyfig: A genome comparison visualizer","volume":"27","author":"Sullivan","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1128\/JB.183.1.358-366.2001","article-title":"Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages","volume":"183","author":"Tetart","year":"2001","journal-title":"J Bacteriol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: Molecular Evolutionary Genetics Analysis Version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"D708","DOI":"10.1093\/nar\/gkx932","article-title":"Virus taxonomy: The database of the International Committee on Taxonomy of Viruses (ICTV)","volume":"46","author":"Lefkowitz","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1128\/MMBR.67.1.86-156.2003","article-title":"Bacteriophage T4 genome","volume":"67","author":"Miller","year":"2003","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1007\/s12275-010-0055-4","article-title":"Phenotypic characterization and genomic analysis of the Shigella sonnei bacteriophage SP18","volume":"48","author":"Kim","year":"2010","journal-title":"J. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1007\/s00705-010-0656-6","article-title":"Low-temperature T4-like coliphages vB_EcoM-VR5, vB_EcoM-VR7 and vB_EcoM-VR20","volume":"155","author":"Kaliniene","year":"2010","journal-title":"Arch. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e0081121","DOI":"10.1128\/mra.00811-21","article-title":"Genome Sequences of Bacteriophages UPEC01, UPEC03, UPEC06, and UPEC07 Infecting Avian Pathogenic Escherichia coli","volume":"11","author":"Kazibwe","year":"2022","journal-title":"Microbiol. Resour. Announc."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Adriaenssens, E., and Brister, J.R. (2017). How to Name and Classify Your Phage: An Informal Guide. Viruses, 9.","DOI":"10.1101\/111526"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2329","DOI":"10.1007\/s007050050246","article-title":"A catalogue of T4-type bacteriophages","volume":"142","author":"Ackermann","year":"1997","journal-title":"Arch. Virol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"8276","DOI":"10.1128\/JB.186.24.8276-8286.2004","article-title":"Comparative genomics of the T4-Like Escherichia coli phage JS98: Implications for the evolution of T4 phages","volume":"186","author":"Canchaya","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2113","DOI":"10.1111\/j.1462-2920.2012.02704.x","article-title":"Phylogenomics of T4 cyanophages: Lateral gene transfer in the 'core' and origins of host genes","volume":"14","author":"Sullivan","year":"2012","journal-title":"Environ. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/S0923-2508(03)00069-X","article-title":"The diversity and evolution of the T4-type bacteriophages","volume":"154","author":"Desplats","year":"2003","journal-title":"Res. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.virol.2009.03.009","article-title":"T4 phages against Escherichia coli diarrhea: Potential and problems","volume":"388","author":"Denou","year":"2009","journal-title":"Virology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/j.virol.2006.12.031","article-title":"Modular architecture of the T4 phage superfamily: A conserved core genome and a plastic periphery","volume":"362","author":"Comeau","year":"2007","journal-title":"Virology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5220","DOI":"10.1128\/JB.185.17.5220-5233.2003","article-title":"Complete genome sequence of the broad-host-range vibriophage KVP40: Comparative genomics of a T4-related bacteriophage","volume":"185","author":"Miller","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1038\/nrmicro2315","article-title":"Bacteriophage resistance mechanisms","volume":"8","author":"Labrie","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"40349","DOI":"10.1038\/srep40349","article-title":"Characterization of two polyvalent phages infecting Enterobacteriaceae","volume":"7","author":"Hamdi","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Lee, H., Ku, H.J., Lee, D.H., Kim, Y.T., Shin, H., Ryu, S., and Lee, J.-H. (2016). Characterization and Genomic Study of the Novel Bacteriophage HY01 Infecting Both Escherichia coli O157:H7 and Shigella flexneri: Potential as a Biocontrol Agent in Food. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0168985"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/12\/2740\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:36:31Z","timestamp":1760146591000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/12\/2740"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,8]]},"references-count":41,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["v14122740"],"URL":"https:\/\/doi.org\/10.3390\/v14122740","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,8]]}}}