Genomic and functional characterization of five novel Salmonella-targeting bacteriophages

Abstract 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 r...

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Main Authors: Marta Kuźmińska-Bajor, Paulina Śliwka, Maciej Ugorski, Paweł Korzeniowski, Aneta Skaradzińska, Maciej Kuczkowski, Magdalena Narajaczyk, Alina Wieliczko, Rafał Kolenda
Format: Article
Language:English
Published: BMC 2021-09-01
Series:Virology Journal
Subjects:
Online Access:https://doi.org/10.1186/s12985-021-01655-4
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author Marta Kuźmińska-Bajor
Paulina Śliwka
Maciej Ugorski
Paweł Korzeniowski
Aneta Skaradzińska
Maciej Kuczkowski
Magdalena Narajaczyk
Alina Wieliczko
Rafał Kolenda
author_facet Marta Kuźmińska-Bajor
Paulina Śliwka
Maciej Ugorski
Paweł Korzeniowski
Aneta Skaradzińska
Maciej Kuczkowski
Magdalena Narajaczyk
Alina Wieliczko
Rafał Kolenda
author_sort Marta Kuźmińska-Bajor
collection DOAJ
description Abstract 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.
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spelling doaj.art-b0b9ed8ef88b4167854cb4cdaac41f762022-12-21T18:40:19ZengBMCVirology Journal1743-422X2021-09-0118111410.1186/s12985-021-01655-4Genomic and functional characterization of five novel Salmonella-targeting bacteriophagesMarta Kuźmińska-Bajor0Paulina Śliwka1Maciej Ugorski2Paweł Korzeniowski3Aneta Skaradzińska4Maciej Kuczkowski5Magdalena Narajaczyk6Alina Wieliczko7Rafał Kolenda8Department of Biotechnology and Food Microbiology, Faculty of Biotechnology and Food Sciences, Wrocław University of Environmental and Life SciencesDepartment of Biotechnology and Food Microbiology, Faculty of Biotechnology and Food Sciences, Wrocław University of Environmental and Life SciencesDepartment of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Wrocław University of Environmental and Life SciencesDepartment of Biotechnology and Food Microbiology, Faculty of Biotechnology and Food Sciences, Wrocław University of Environmental and Life SciencesDepartment of Biotechnology and Food Microbiology, Faculty of Biotechnology and Food Sciences, Wrocław University of Environmental and Life SciencesDepartment of Epizootiology and Clinic of Birds and Exotic Animals, Faculty of Veterinary Medicine, Wrocław University of Environmental and Life SciencesDepartment of Electron Microscopy, Faculty of Biology, University of GdanskDepartment of Epizootiology and Clinic of Birds and Exotic Animals, Faculty of Veterinary Medicine, Wrocław University of Environmental and Life SciencesDepartment of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Wrocław University of Environmental and Life SciencesAbstract 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.https://doi.org/10.1186/s12985-021-01655-4Salmonella entericaBacteriophagesBacteriophage geneticsComparative genomics
spellingShingle Marta Kuźmińska-Bajor
Paulina Śliwka
Maciej Ugorski
Paweł Korzeniowski
Aneta Skaradzińska
Maciej Kuczkowski
Magdalena Narajaczyk
Alina Wieliczko
Rafał Kolenda
Genomic and functional characterization of five novel Salmonella-targeting bacteriophages
Virology Journal
Salmonella enterica
Bacteriophages
Bacteriophage genetics
Comparative genomics
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 Salmonella enterica
Bacteriophages
Bacteriophage genetics
Comparative genomics
url https://doi.org/10.1186/s12985-021-01655-4
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