{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T16:18:32Z","timestamp":1781885912339,"version":"3.54.5"},"reference-count":52,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2020,11,21]],"date-time":"2020-11-21T00:00:00Z","timestamp":1605916800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2017\/27\/B\/NZ9\/00393"],"award-info":[{"award-number":["2017\/27\/B\/NZ9\/00393"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Two newly discovered bacteriophages, isolated from chicken feces and infecting Salmonella enterica strains, are described in this report. These phages have been named vB_Sen-TO17 and vB_Sen-E22, and we present their molecular and functional characterization. Both studied viruses are able to infect several S. enterica strains and develop lytically, but their specific host ranges differ significantly. Electron microscopic analyses of virions have been performed, and full genome sequences were determined and characterized, along with molecular phylogenetic studies. Genomes of vB_Sen-TO17 (ds DNA of 41,658 bp) and vB_Sen-E22 (dsDNA of 108,987 bp) are devoid of homologs of any known or putative gene coding for toxins or any other proteins potentially deleterious for eukaryotic cells. Both phages adsorbed efficiently (&gt;95% adsorbed virions) within 10 min at 42 \u00b0C (resembling chicken body temperature) on cells of most tested host strains. Kinetics of lytic development of vB_Sen-TO17 and vB_Sen-E22, determined in one-step growth experiments, indicated that development is complete within 30\u201340 min at 42 \u00b0C, whereas burst sizes vary from 9 to 79 progeny phages per cell for vB_Sen-TO17 and from 18 to 64 for vB_Sen-E22, depending on the host strain. Virions of both phages were relatively stable (from several percent to almost 100% survivability) under various conditions, including acidic and alkaline pH values (from 3 to 12), temperatures from \u221280 \u00b0C to 60 \u00b0C, 70% ethanol, chloroform, and 10% DMSO. These characteristics of vB_Sen-TO17 and vB_Sen-E22 indicate that these phages might be considered in further studies on phage therapy, particularly in attempts to eliminate S. enterica from chicken intestine.<\/jats:p>","DOI":"10.3390\/ijms21228821","type":"journal-article","created":{"date-parts":[[2020,11,23]],"date-time":"2020-11-23T01:28:48Z","timestamp":1606094928000},"page":"8821","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Bacteriophages vB_Sen-TO17 and vB_Sen-E22, Newly Isolated Viruses from Chicken Feces, Specific for Several Salmonella enterica Strains"],"prefix":"10.3390","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5023-1531","authenticated-orcid":false,"given":"Katarzyna","family":"Kosznik-Kwa\u015bnicka","sequence":"first","affiliation":[{"name":"Laboratory of Molecular Biology, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, K\u0142adki 24, 80-822 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3746-8726","authenticated-orcid":false,"given":"\u0141ukasz","family":"Grabowski","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Biology, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, K\u0142adki 24, 80-822 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Micha\u0142","family":"Grabski","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland"},{"name":"Institute of Oceanology, Polish Academy of Sciences, Powsta\u0144c\u00f3w Warszawy 55, 81-712 Sopot, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mateusz","family":"Kaszubski","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7568-7818","authenticated-orcid":false,"given":"Marcin","family":"G\u00f3rniak","sequence":"additional","affiliation":[{"name":"Department of Molecular Evolution, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agata","family":"Jurczak-Kurek","sequence":"additional","affiliation":[{"name":"Department of Molecular Evolution, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4042-7466","authenticated-orcid":false,"given":"Grzegorz","family":"W\u0119grzyn","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alicja","family":"W\u0119grzyn","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Biology, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, K\u0142adki 24, 80-822 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,11,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2852","DOI":"10.1002\/btpr.2852","article-title":"Economic evaluation of the development of a phage therapy product for the control of Salmonella in poultry","volume":"35","author":"Clavijo","year":"2019","journal-title":"Biotechnol. Progr."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1006","DOI":"10.3382\/ps\/pex359","article-title":"The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: A review","volume":"97","author":"Clavijo","year":"2018","journal-title":"Poult. Sci."},{"key":"ref_3","first-page":"391","article-title":"Same species, different diseases: How and why typhoidal and non-typhoidal Salmonella enterica serovars differ","volume":"5","author":"Boyle","year":"2014","journal-title":"Front. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1128\/MMBR.00016-10","article-title":"Origins and evolution of antibiotic resistance","volume":"74","author":"Davies","year":"2010","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/s40985-018-0099-2","article-title":"Food safety impacts of antimicrobial use and their residues in aquaculture","volume":"39","author":"Okocha","year":"2018","journal-title":"Public Health Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.mib.2019.10.008","article-title":"Antibiotics: Past, present and future","volume":"51","author":"Hutchings","year":"2019","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"96","DOI":"10.3109\/03009734.2014.901445","article-title":"Antibiotic resistance\u2014Consequences for animal health, welfare, and food production","volume":"119","author":"Bengtsson","year":"2014","journal-title":"Upsala J. Med. Sci."},{"key":"ref_8","first-page":"277","article-title":"The antibiotic resistance crisis: Part 1: Causes and threats","volume":"40","author":"Ventola","year":"2015","journal-title":"Pharm. Therapeut."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1115","DOI":"10.1080\/14712598.2019.1651287","article-title":"The fall and rise of phage therapy in modern medicine","volume":"19","author":"Borysowski","year":"2019","journal-title":"Expert Opin. Biol. Ther."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1002\/med.21593","article-title":"Phage therapy: Current status and perspectives","volume":"40","author":"Borysowski","year":"2020","journal-title":"Med. Resr Rev."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Rohde, C., Resch, G., Pirnay, J.P., Blasdel, B.G., Debarbieux, L., Gelman, D., G\u00f3rski, A., Hazan, R., Huys, I., and Kakabadze, E. (2018). Expert opinion on three phage therapy related topics: Bacterial phage resistance, phage training and prophages in bacterial production strains. Viruses, 10.","DOI":"10.3390\/v10040178"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Yan, T., Liang, L., Yin, P., Zhou, Y., Sharoba, A.M., Lu, Q., Dong, X., Liu, K., Connerton, I.F., and Li, J. (2020). Application of a novel phage LPSEYT for biological control of Salmonella in foods. Microorganisms, 8.","DOI":"10.3390\/microorganisms8030400"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Kakabadze, E., Makalatia, K., Grdzelishvili, N., Bakuradze, N., Goderdzishvili, M., Kusradze, I., Phoba, M.F., Lunguya, O., Lood, C., and Lavigne, R. (2018). Selection of potential therapeutic bacteriophages that lyse a CTX-M-15 extended spectrum \u03b2-lactamase producing Salmonella enterica serovar Typhi strain from the Democratic Republic of the Congo. Viruses, 10.","DOI":"10.3390\/v10040172"},{"key":"ref_14","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_15","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1007\/s11262-018-1538-3","article-title":"Genomics of Salmonella phage \u03a6Stp1: Candidate bacteriophage for biocontrol","volume":"54","author":"Sritha","year":"2018","journal-title":"Virus Genes"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1139\/cjm-2017-0740","article-title":"Three Salmonella enterica serovar Enteritidis bacteriophages from the Siphoviridae family are promising candidates for phage therapy","volume":"6","author":"Chen","year":"2018","journal-title":"Can. J. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e01160-19","DOI":"10.1128\/MRA.01160-19","article-title":"Complete genome sequence of Salmonella enterica serovar Typhimurium siphophage Seabear","volume":"8","author":"Patil","year":"2019","journal-title":"Microbiol. Resour. Announc."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Holgu\u00edn, A.V., C\u00e1rdenas, P., Prada-Pe\u00f1aranda, C., Rabelo Leite, L., Buitrago, C., Clavijo, V., Oliveira, G., Leekitcharoenphon, P., M\u00f8ller Aarestrup, F., and Vives, M.J. (2019). Host resistance, genomics and population dynamics in a Salmonella Enteritidis and phage system. Viruses, 11.","DOI":"10.3390\/v11020188"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"103659","DOI":"10.1016\/j.micpath.2019.103659","article-title":"Morphologic and genomic characterization of a broad host range Salmonella enterica serovar Pullorum lytic phage vB_SPuM_SP116","volume":"136","author":"Bao","year":"2019","journal-title":"Microb. Pathog."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Mohamed, A., Taha, O., El-Sherif, H.M., Connerton, P.L., Hooton, S.P.T., Bassim, N.D., Connerton, I., and El-Shibiny, A. (2020). Bacteriophage ZCSE2 is a potent antimicrobial against Salmonella enterica serovars: Ultrastructure, genomics and efficacy. Viruses, 12.","DOI":"10.3390\/v12040424"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Kosznik-Kwa\u015bnicka, K., Ciemi\u0144ska, K., Grabski, M., Grabowski, \u0141., G\u00f3rniak, M., Jurczak-Kurek, A., W\u0119grzyn, G., and W\u0119grzyn, A. (2020). Characteristics of a series of three bacteriophages infecting Salmonella enterica strains. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21176152"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"4367","DOI":"10.3382\/ps\/pey294","article-title":"Autophage as a control measure for Salmonella in laying hens","volume":"97","author":"Vega","year":"2018","journal-title":"Poult. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1007\/s11262-018-1549-0","article-title":"Isolation and identification of Salmonella pullorum bacteriophage YSP2 and its use as a therapy for chicken diarrhea","volume":"54","author":"Tie","year":"2018","journal-title":"Virus Genes"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"5054","DOI":"10.3382\/ps\/pez251","article-title":"Phage cocktail SalmoFREE\u00ae reduces Salmonella on a commercial broiler farm","volume":"98","author":"Clavijo","year":"2019","journal-title":"Poult. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"108527","DOI":"10.1016\/j.vetmic.2019.108527","article-title":"Effect of time of therapy with wild-type lytic bacteriophages on the reduction of Salmonella Enteritidis in broiler chickens","volume":"240","author":"Vaz","year":"2020","journal-title":"Vet. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3643","DOI":"10.1016\/j.psj.2020.03.051","article-title":"Broad-host-range Salmonella bacteriophage STP4-a and its potential application evaluation in poultry industry","volume":"99","author":"Li","year":"2020","journal-title":"Poult. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"\u017bbikowska, K., Michalczuk, M., and Dolka, B. (2020). The use of bacteriophages in the poultry industry. Animals, 10.","DOI":"10.3390\/ani10050872"},{"key":"ref_28","first-page":"131","article-title":"Phage therapy: Assessment of the efficacy of a bacteriophage isolated in the treatment of salmonellosis induced by Salmonella Enteritidis in mice","volume":"10","author":"Nikkhahi","year":"2017","journal-title":"Gastroenterol. Hepatol. Bed Bench"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.micpath.2018.10.042","article-title":"Isolation and characterization of a broad-spectrum phage of multiple drug resistant Salmonella and its therapeutic utility in mice","volume":"126","author":"Tang","year":"2019","journal-title":"Microb. Pathog."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"20190290","DOI":"10.1590\/0037-8682-0290-2019","article-title":"Phage therapy as an approach to control Salmonella enterica serotype Enteritidis infection in mice","volume":"52","author":"Dallal","year":"2019","journal-title":"Rev. Soc. Bras. Med. Trop."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"126471","DOI":"10.1016\/j.micres.2020.126471","article-title":"The complete genome of lytic Salmonella phage vB_SenM-PA13076 and therapeutic potency in the treatment of lethal Salmonella Enteritidis infections in mice","volume":"237","author":"Bao","year":"2020","journal-title":"Microbiol. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1292\/jvms.17-0501","article-title":"Evaluation of the broad-spectrum lytic capability of bacteriophage cocktails against various Salmonella serovars and their effects on weaned pigs infected with Salmonella Typhimurium","volume":"80","author":"Seo","year":"2018","journal-title":"J. Vet. Med. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1002\/jobm.201800412","article-title":"Bacteriophages: An overview of the control strategies against multiple bacterial infections in different fields","volume":"59","author":"Jamal","year":"2019","journal-title":"J. Basic Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"34338","DOI":"10.1038\/srep34338","article-title":"Biodiversity of bacteriophages: Morphological and biological properties of a large group of phages isolated from urban sewage","volume":"6","author":"Bloch","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_35","first-page":"1177","article-title":"Bacteriophage procurement for therapeutic purposes","volume":"7","author":"Zaczek","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_36","unstructured":"Sambrook, J.F., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor. [3rd ed.]."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/0027-5107(83)90143-4","article-title":"Curing and induction of the Fels 1 and Fels 2 prophages in the Ames mutagen tester strains of Salmonella typhimurium","volume":"110","author":"Affolter","year":"1983","journal-title":"Mutat. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1046\/j.1365-2958.1999.01461.x","article-title":"Inducible prophages contribute to Salmonella virulence in mice","volume":"33","author":"Bossi","year":"1999","journal-title":"Mol. Microbiol."},{"key":"ref_39","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_40","doi-asserted-by":"crossref","first-page":"3326","DOI":"10.3389\/fmicb.2018.03326","article-title":"Characterization of bacteriophage VB-EcoS-95, isolated from urban sewage and revealing extremely rapid lytic development","volume":"9","author":"Topka","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/1477-3155-5-10","article-title":"Stability and assembly in vitro of bacteriophage PP7 virus-like particles","volume":"5","author":"Caldeira","year":"2007","journal-title":"J. Nanobiotechnol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: Rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"D225","DOI":"10.1093\/nar\/gkq1189","article-title":"CDD: A conserved Domain database for the functional annotation of proteins","volume":"39","author":"Lu","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"W29","DOI":"10.1093\/nar\/gkr367","article-title":"HMMER web server: Interactive sequence similarity searching","volume":"39","author":"Finn","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"11","DOI":"10.4161\/rna.8.1.13346","article-title":"ARNold: A web tool for the prediction of Rho-independent transcription terminators","volume":"8","author":"Naville","year":"2011","journal-title":"RNA Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1093\/bioinformatics\/bts014","article-title":"PHACTS, a computational approach to classifying the lifestyle of phages","volume":"28","author":"McNair","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"8292","DOI":"10.1038\/s41598-017-07910-5","article-title":"PhageTerm: A tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data","volume":"7","author":"Garneau","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1093\/bioinformatics\/bti054","article-title":"Circular genome visualization and exploration using CGView","volume":"21","author":"Stothard","year":"2005","journal-title":"Bioinformatics"},{"key":"ref_49","first-page":"543","article-title":"SeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny","volume":"12","author":"Gautier","year":"1996","journal-title":"Comput. Appl. Biosci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1394","DOI":"10.1101\/gr.2289704","article-title":"Mauve: Multiple alignment of conserved genomic sequence with rearrangements","volume":"14","author":"Darling","year":"2004","journal-title":"Genome Res."},{"key":"ref_51","unstructured":"Swofford, D.L. (2003). Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4, Sinauer Associates."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1618","DOI":"10.1093\/molbev\/msw042","article-title":"Efficiencies of the NJp, maximum likelihood, and Bayesian methods of phyogenetic construction for compositional and noncompositional genes","volume":"33","author":"Yoshida","year":"2016","journal-title":"Mol. Biol. Evol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/22\/8821\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:35:29Z","timestamp":1760178929000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/22\/8821"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,11,21]]},"references-count":52,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2020,11]]}},"alternative-id":["ijms21228821"],"URL":"https:\/\/doi.org\/10.3390\/ijms21228821","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,21]]}}}