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Genomic and functional characterization of five novel Salmonella-targeting bacteriophages

BACKGROUND: The host-unrestricted, non-typhoidal Salmonella enterica serovar Enteritidis (S. Enteritidis) and the serovar Typhimurium (S. Typhimurium) are major causative agents of food-borne gastroenteritis, and the host-restricted Salmonella enterica serovar Gallinarum (S. Gallinarum) is responsib...

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Autores principales: Kuźmińska-Bajor, Marta, Śliwka, Paulina, Ugorski, Maciej, Korzeniowski, Paweł, Skaradzińska, Aneta, Kuczkowski, Maciej, Narajaczyk, Magdalena, Wieliczko, Alina, Kolenda, Rafał
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8425127/
https://www.ncbi.nlm.nih.gov/pubmed/34496915
http://dx.doi.org/10.1186/s12985-021-01655-4
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author Kuźmińska-Bajor, Marta
Śliwka, Paulina
Ugorski, Maciej
Korzeniowski, Paweł
Skaradzińska, Aneta
Kuczkowski, Maciej
Narajaczyk, Magdalena
Wieliczko, Alina
Kolenda, Rafał
author_facet Kuźmińska-Bajor, Marta
Śliwka, Paulina
Ugorski, Maciej
Korzeniowski, Paweł
Skaradzińska, Aneta
Kuczkowski, Maciej
Narajaczyk, Magdalena
Wieliczko, Alina
Kolenda, Rafał
author_sort Kuźmińska-Bajor, Marta
collection PubMed
description BACKGROUND: The host-unrestricted, non-typhoidal Salmonella enterica serovar Enteritidis (S. Enteritidis) and the serovar Typhimurium (S. Typhimurium) are major causative agents of food-borne gastroenteritis, and the host-restricted Salmonella enterica serovar Gallinarum (S. Gallinarum) is responsible for fowl typhoid. Increasing drug resistance in Salmonella contributes to the reduction of effective therapeutic and/or preventive options. Bacteriophages appear to be promising antibacterial tools, able to combat infectious diseases caused by a wide range of Salmonella strains belonging to both host-unrestricted and host-restricted Salmonella serovars. METHODS: In this study, five novel lytic Salmonella phages, named UPWr_S1-5, were isolated and characterized, including host range determination by plaque formation, morphology visualization with transmission electron microscopy, and establishment of physiological parameters. Moreover, phage genomes were sequenced, annotated and analyzed, and their genomes were compared with reference Salmonella phages by use of average nucleotide identity, phylogeny, dot plot, single nucleotide variation and protein function analysis. RESULTS: It was found that UPWr_S1-5 phages belong to the genus Jerseyvirus within the Siphoviridae family. All UPWr_S phages were found to efficiently infect various Salmonella serovars. Host range determination revealed differences in host infection profiles and exhibited ability to infect Salmonella enterica serovars such as Enteritidis, Gallinarum, Senftenberg, Stanley and Chester. The lytic life cycle of UPWr_S phages was confirmed using the mitomycin C test assay. Genomic analysis revealed that genomes of UPWr_S phages are composed of 51 core and 19 accessory genes, with 33 of all predicted genes having assigned functions. UPWr_S genome organization comparison revealed 3 kinds of genomes and mosaic structure. UPWr_S phages showed very high sequence similarity to each other, with more than 95% average nucleotide identity. CONCLUSIONS: Five novel UPWr_S1-5 bacteriophages were isolated and characterized. They exhibit host lysis range within 5 different serovars and are efficient in lysis of both host-unrestricted and host-restricted Salmonella serovars. Therefore, because of their ability to infect various Salmonella serovars and lytic life cycle, UPWr_S1-5 phages can be considered as useful tools in biological control of salmonellosis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12985-021-01655-4.
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spelling pubmed-84251272021-09-10 Genomic and functional characterization of five novel Salmonella-targeting bacteriophages Kuźmińska-Bajor, Marta Śliwka, Paulina Ugorski, Maciej Korzeniowski, Paweł Skaradzińska, Aneta Kuczkowski, Maciej Narajaczyk, Magdalena Wieliczko, Alina Kolenda, Rafał Virol J Research BACKGROUND: The host-unrestricted, non-typhoidal Salmonella enterica serovar Enteritidis (S. Enteritidis) and the serovar Typhimurium (S. Typhimurium) are major causative agents of food-borne gastroenteritis, and the host-restricted Salmonella enterica serovar Gallinarum (S. Gallinarum) is responsible for fowl typhoid. Increasing drug resistance in Salmonella contributes to the reduction of effective therapeutic and/or preventive options. Bacteriophages appear to be promising antibacterial tools, able to combat infectious diseases caused by a wide range of Salmonella strains belonging to both host-unrestricted and host-restricted Salmonella serovars. METHODS: In this study, five novel lytic Salmonella phages, named UPWr_S1-5, were isolated and characterized, including host range determination by plaque formation, morphology visualization with transmission electron microscopy, and establishment of physiological parameters. Moreover, phage genomes were sequenced, annotated and analyzed, and their genomes were compared with reference Salmonella phages by use of average nucleotide identity, phylogeny, dot plot, single nucleotide variation and protein function analysis. RESULTS: It was found that UPWr_S1-5 phages belong to the genus Jerseyvirus within the Siphoviridae family. All UPWr_S phages were found to efficiently infect various Salmonella serovars. Host range determination revealed differences in host infection profiles and exhibited ability to infect Salmonella enterica serovars such as Enteritidis, Gallinarum, Senftenberg, Stanley and Chester. The lytic life cycle of UPWr_S phages was confirmed using the mitomycin C test assay. Genomic analysis revealed that genomes of UPWr_S phages are composed of 51 core and 19 accessory genes, with 33 of all predicted genes having assigned functions. UPWr_S genome organization comparison revealed 3 kinds of genomes and mosaic structure. UPWr_S phages showed very high sequence similarity to each other, with more than 95% average nucleotide identity. CONCLUSIONS: Five novel UPWr_S1-5 bacteriophages were isolated and characterized. They exhibit host lysis range within 5 different serovars and are efficient in lysis of both host-unrestricted and host-restricted Salmonella serovars. Therefore, because of their ability to infect various Salmonella serovars and lytic life cycle, UPWr_S1-5 phages can be considered as useful tools in biological control of salmonellosis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12985-021-01655-4. BioMed Central 2021-09-08 /pmc/articles/PMC8425127/ /pubmed/34496915 http://dx.doi.org/10.1186/s12985-021-01655-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Kuźmińska-Bajor, Marta
Śliwka, Paulina
Ugorski, Maciej
Korzeniowski, Paweł
Skaradzińska, Aneta
Kuczkowski, Maciej
Narajaczyk, Magdalena
Wieliczko, Alina
Kolenda, Rafał
Genomic and functional characterization of five novel Salmonella-targeting bacteriophages
title Genomic and functional characterization of five novel Salmonella-targeting bacteriophages
title_full Genomic and functional characterization of five novel Salmonella-targeting bacteriophages
title_fullStr Genomic and functional characterization of five novel Salmonella-targeting bacteriophages
title_full_unstemmed Genomic and functional characterization of five novel Salmonella-targeting bacteriophages
title_short Genomic and functional characterization of five novel Salmonella-targeting bacteriophages
title_sort genomic and functional characterization of five novel salmonella-targeting bacteriophages
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8425127/
https://www.ncbi.nlm.nih.gov/pubmed/34496915
http://dx.doi.org/10.1186/s12985-021-01655-4
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