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Broad host range bacteriophage, EscoHU1, infecting Escherichia coli O157:H7 and Salmonella enterica: Characterization, comparative genomics, and applications in food safety
Shiga toxin-producing Escherichia coli and Salmonella enterica are important pathogens worldwide. Bacteriophages can be effectively used to reduce the incidence of foodborne pathogens. The host recognition systems of phages are highly specific, with the host range of a common phage being limited to...
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Published in: | International journal of food microbiology 2022-07, Vol.372, p.109680-109680, Article 109680 |
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description | Shiga toxin-producing Escherichia coli and Salmonella enterica are important pathogens worldwide. Bacteriophages can be effectively used to reduce the incidence of foodborne pathogens. The host recognition systems of phages are highly specific, with the host range of a common phage being limited to the species or strain level. Here, we characterized a novel broad-host-range phage, EscoHU1, that infects several bacterial species, including E. coli and S. enterica, and evaluated its antimicrobial potential to inhibit E. coli O157:H7 and S. Typhimurium growth in food systems. The adsorption of EscoHU1 on E. coli was faster than that on S. Typhimurium; however, the one-step growth curves of EscoHU1 in both species were similar. Genomic analysis of EscoHU1 revealed that this phage has long direct terminal repeats at both ends of the genome, and phylogenetic analysis of the terminase large subunit confirmed that EscoHU1 belongs to the genus Epseptimavirus. Comparative analysis of structural proteins indicated a diversity of proteins related to the host range (receptor-binding proteins and L-shaped tail fibers). Challenge tests using beef and milk demonstrated the antimicrobial effects of EscoHU1 in inhibiting the growth of E. coli O157:H7 and S. Typhimurium in the food system. However, the antimicrobial effect of EscoHU1 on S. Typhimurium was lower than that on E. coli O157:H7. These results suggest that the novel broad-host-range phage EscoHU1 may serve as an effective antimicrobial agent to reduce food poisoning caused by E. coli O157:H7 and S. Typhimurium.
•The broad host range phage EscoHU1 was characterized.•Phage EscoHU1 belongs to the genus Epseptimavirus.•Receptor-binding protein and L-shaped tail fiber show high diversity.•Phage EscoHU1 can inhibit E. coli and S. Typhimurium growth in food. |
doi_str_mv | 10.1016/j.ijfoodmicro.2022.109680 |
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•The broad host range phage EscoHU1 was characterized.•Phage EscoHU1 belongs to the genus Epseptimavirus.•Receptor-binding protein and L-shaped tail fiber show high diversity.•Phage EscoHU1 can inhibit E. coli and S. Typhimurium growth in food.</description><identifier>ISSN: 0168-1605</identifier><identifier>EISSN: 1879-3460</identifier><identifier>DOI: 10.1016/j.ijfoodmicro.2022.109680</identifier><identifier>PMID: 35512432</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Antiinfectives and antibacterials ; Antimicrobial agents ; Bacteriophages - genetics ; Broad host range phage ; Cattle ; Comparative analysis ; Demerecviridae ; E coli ; Epseptimavirus ; Escherichia coli ; Escherichia coli O157 ; Fibers ; Food ; Food contamination ; Food Microbiology ; Food poisoning ; Food Safety ; Food systems ; Foodborne pathogens ; Genomic analysis ; Genomics ; Growth curves ; Host range ; Host Specificity ; Pathogens ; Phage utilization ; Phages ; Phylogeny ; Proteins ; Salmonella ; Salmonella enterica ; Shiga toxin ; Species ; Structural proteins ; Tail fiber protein ; Terminase ; Toxins</subject><ispartof>International journal of food microbiology, 2022-07, Vol.372, p.109680-109680, Article 109680</ispartof><rights>2022 Elsevier B.V.</rights><rights>Copyright © 2022 Elsevier B.V. All rights reserved.</rights><rights>Copyright Elsevier BV Jul 2, 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c522t-5293aea8570f2b2acb340734387dae7cb312bbcc3fb86542df78bcfb38e607e23</citedby><cites>FETCH-LOGICAL-c522t-5293aea8570f2b2acb340734387dae7cb312bbcc3fb86542df78bcfb38e607e23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35512432$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yamaki, Shogo</creatorcontrib><creatorcontrib>Yamazaki, Koji</creatorcontrib><creatorcontrib>Kawai, Yuji</creatorcontrib><title>Broad host range bacteriophage, EscoHU1, infecting Escherichia coli O157:H7 and Salmonella enterica: Characterization, comparative genomics, and applications in food safety</title><title>International journal of food microbiology</title><addtitle>Int J Food Microbiol</addtitle><description>Shiga toxin-producing Escherichia coli and Salmonella enterica are important pathogens worldwide. Bacteriophages can be effectively used to reduce the incidence of foodborne pathogens. The host recognition systems of phages are highly specific, with the host range of a common phage being limited to the species or strain level. Here, we characterized a novel broad-host-range phage, EscoHU1, that infects several bacterial species, including E. coli and S. enterica, and evaluated its antimicrobial potential to inhibit E. coli O157:H7 and S. Typhimurium growth in food systems. The adsorption of EscoHU1 on E. coli was faster than that on S. Typhimurium; however, the one-step growth curves of EscoHU1 in both species were similar. Genomic analysis of EscoHU1 revealed that this phage has long direct terminal repeats at both ends of the genome, and phylogenetic analysis of the terminase large subunit confirmed that EscoHU1 belongs to the genus Epseptimavirus. Comparative analysis of structural proteins indicated a diversity of proteins related to the host range (receptor-binding proteins and L-shaped tail fibers). Challenge tests using beef and milk demonstrated the antimicrobial effects of EscoHU1 in inhibiting the growth of E. coli O157:H7 and S. Typhimurium in the food system. However, the antimicrobial effect of EscoHU1 on S. Typhimurium was lower than that on E. coli O157:H7. These results suggest that the novel broad-host-range phage EscoHU1 may serve as an effective antimicrobial agent to reduce food poisoning caused by E. coli O157:H7 and S. Typhimurium.
•The broad host range phage EscoHU1 was characterized.•Phage EscoHU1 belongs to the genus Epseptimavirus.•Receptor-binding protein and L-shaped tail fiber show high diversity.•Phage EscoHU1 can inhibit E. coli and S. Typhimurium growth in food.</description><subject>Animals</subject><subject>Antiinfectives and antibacterials</subject><subject>Antimicrobial agents</subject><subject>Bacteriophages - genetics</subject><subject>Broad host range phage</subject><subject>Cattle</subject><subject>Comparative analysis</subject><subject>Demerecviridae</subject><subject>E coli</subject><subject>Epseptimavirus</subject><subject>Escherichia coli</subject><subject>Escherichia coli O157</subject><subject>Fibers</subject><subject>Food</subject><subject>Food contamination</subject><subject>Food Microbiology</subject><subject>Food poisoning</subject><subject>Food Safety</subject><subject>Food systems</subject><subject>Foodborne pathogens</subject><subject>Genomic analysis</subject><subject>Genomics</subject><subject>Growth curves</subject><subject>Host range</subject><subject>Host Specificity</subject><subject>Pathogens</subject><subject>Phage utilization</subject><subject>Phages</subject><subject>Phylogeny</subject><subject>Proteins</subject><subject>Salmonella</subject><subject>Salmonella enterica</subject><subject>Shiga toxin</subject><subject>Species</subject><subject>Structural proteins</subject><subject>Tail fiber protein</subject><subject>Terminase</subject><subject>Toxins</subject><issn>0168-1605</issn><issn>1879-3460</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNqNkc1u1DAUhSMEotPCKyAjNiwmg3_i_HRXRoVBqtQFdG05zs3EUWIHO1OpPBMP2RtSEGLFxpavvnOu7z1J8pbRHaMs_9DvbN9634zWBL_jlHOsV3lJnyUbVhZVKrKcPk82yJYpy6k8S85j7CmlUgj6MjkTUjKeCb5Jfn4MXjek83EmQbsjkFqbGYL1U6ePsCXX0fjDHdsS61ows3XHpdQhYTqrifGDJbdMFpeHgmjXkK96GL2DYdAE3GJk9CXZdzqstj_0bL3bom6csDbbeyBHcB5HidtfBnqaBhQtWMSmZBmURN3C_PAqedHqIcLrp_siuft0_W1_SG9uP3_ZX92kRnI-p5JXQoMuZUFbXnNtapHRQmSiLBoNBT4Zr2tjRFuXucx40xZlbdpalJDTAri4SN6vvlPw308QZzXaaJaZHPhTVDzPcd_LMhF99w_a-1Nw-DukSkkriSdS1UphXjEGaNUU7KjDg2JULZGqXv0VqVoiVWukqH3z1OFUj9D8Uf7OEIH9CgCu5N5CUNFYcAYaGzAx1Xj7H20eAbtjug4</recordid><startdate>20220702</startdate><enddate>20220702</enddate><creator>Yamaki, Shogo</creator><creator>Yamazaki, Koji</creator><creator>Kawai, Yuji</creator><general>Elsevier B.V</general><general>Elsevier BV</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7QR</scope><scope>7T7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20220702</creationdate><title>Broad host range bacteriophage, EscoHU1, infecting Escherichia coli O157:H7 and Salmonella enterica: Characterization, comparative genomics, and applications in food safety</title><author>Yamaki, Shogo ; Yamazaki, Koji ; Kawai, Yuji</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c522t-5293aea8570f2b2acb340734387dae7cb312bbcc3fb86542df78bcfb38e607e23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Antiinfectives and antibacterials</topic><topic>Antimicrobial agents</topic><topic>Bacteriophages - genetics</topic><topic>Broad host range phage</topic><topic>Cattle</topic><topic>Comparative analysis</topic><topic>Demerecviridae</topic><topic>E coli</topic><topic>Epseptimavirus</topic><topic>Escherichia coli</topic><topic>Escherichia coli O157</topic><topic>Fibers</topic><topic>Food</topic><topic>Food contamination</topic><topic>Food Microbiology</topic><topic>Food poisoning</topic><topic>Food Safety</topic><topic>Food systems</topic><topic>Foodborne pathogens</topic><topic>Genomic analysis</topic><topic>Genomics</topic><topic>Growth curves</topic><topic>Host range</topic><topic>Host Specificity</topic><topic>Pathogens</topic><topic>Phage utilization</topic><topic>Phages</topic><topic>Phylogeny</topic><topic>Proteins</topic><topic>Salmonella</topic><topic>Salmonella enterica</topic><topic>Shiga toxin</topic><topic>Species</topic><topic>Structural proteins</topic><topic>Tail fiber protein</topic><topic>Terminase</topic><topic>Toxins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yamaki, Shogo</creatorcontrib><creatorcontrib>Yamazaki, Koji</creatorcontrib><creatorcontrib>Kawai, Yuji</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>International journal of food microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yamaki, Shogo</au><au>Yamazaki, Koji</au><au>Kawai, Yuji</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Broad host range bacteriophage, EscoHU1, infecting Escherichia coli O157:H7 and Salmonella enterica: Characterization, comparative genomics, and applications in food safety</atitle><jtitle>International journal of food microbiology</jtitle><addtitle>Int J Food Microbiol</addtitle><date>2022-07-02</date><risdate>2022</risdate><volume>372</volume><spage>109680</spage><epage>109680</epage><pages>109680-109680</pages><artnum>109680</artnum><issn>0168-1605</issn><eissn>1879-3460</eissn><abstract>Shiga toxin-producing Escherichia coli and Salmonella enterica are important pathogens worldwide. Bacteriophages can be effectively used to reduce the incidence of foodborne pathogens. The host recognition systems of phages are highly specific, with the host range of a common phage being limited to the species or strain level. Here, we characterized a novel broad-host-range phage, EscoHU1, that infects several bacterial species, including E. coli and S. enterica, and evaluated its antimicrobial potential to inhibit E. coli O157:H7 and S. Typhimurium growth in food systems. The adsorption of EscoHU1 on E. coli was faster than that on S. Typhimurium; however, the one-step growth curves of EscoHU1 in both species were similar. Genomic analysis of EscoHU1 revealed that this phage has long direct terminal repeats at both ends of the genome, and phylogenetic analysis of the terminase large subunit confirmed that EscoHU1 belongs to the genus Epseptimavirus. Comparative analysis of structural proteins indicated a diversity of proteins related to the host range (receptor-binding proteins and L-shaped tail fibers). Challenge tests using beef and milk demonstrated the antimicrobial effects of EscoHU1 in inhibiting the growth of E. coli O157:H7 and S. Typhimurium in the food system. However, the antimicrobial effect of EscoHU1 on S. Typhimurium was lower than that on E. coli O157:H7. These results suggest that the novel broad-host-range phage EscoHU1 may serve as an effective antimicrobial agent to reduce food poisoning caused by E. coli O157:H7 and S. Typhimurium.
•The broad host range phage EscoHU1 was characterized.•Phage EscoHU1 belongs to the genus Epseptimavirus.•Receptor-binding protein and L-shaped tail fiber show high diversity.•Phage EscoHU1 can inhibit E. coli and S. Typhimurium growth in food.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>35512432</pmid><doi>10.1016/j.ijfoodmicro.2022.109680</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Antiinfectives and antibacterials Antimicrobial agents Bacteriophages - genetics Broad host range phage Cattle Comparative analysis Demerecviridae E coli Epseptimavirus Escherichia coli Escherichia coli O157 Fibers Food Food contamination Food Microbiology Food poisoning Food Safety Food systems Foodborne pathogens Genomic analysis Genomics Growth curves Host range Host Specificity Pathogens Phage utilization Phages Phylogeny Proteins Salmonella Salmonella enterica Shiga toxin Species Structural proteins Tail fiber protein Terminase Toxins |
title | Broad host range bacteriophage, EscoHU1, infecting Escherichia coli O157:H7 and Salmonella enterica: Characterization, comparative genomics, and applications in food safety |
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