Genomic and functional characterization of five novel <i>Salmonella</i>-targeting bacteriophages

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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.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12985-021-01655-4.

Related collections

Most cited references 2

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Isolation and characterization of five lytic bacteriophages infecting aVibriostrain closely related toVibrio owensii

Yan-Ping Yu, Ting Gong, Günter Jost … (2013)

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Complete genomic sequence of Salmonella enterica serovar Enteritidis phage SE2.

Shukho Kim, Kiran B. Tiwari, Jungmin Kim (2012)

Salmonella enterica serovar Enteritidis has remained a major food-borne pathogen in humans. We isolated a virulent S. enterica serovar Enteritidis bacteriophage, SE2, which belongs to the family Siphoviridae. Phage SE2 could lyse S. enterica serovar Enteritidis PT-4, and its virulence was maintained even at ambient temperature. The genomic sequence of phage SE2 was composed of 43,221 bp with close similarity to those of Salmonella phage SETP3 and Salmonella phage SS3e. The strong and stable lytic activity of this phage might enable its use as a therapeutic or biocontrol agent against S. enterica serovar Enteritidis.

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Author and article information

Contributors

Marta Kuźmińska-Bajor:

ORCID: http://orcid.org/0000-0003-1904-1059

marta.kuzminska-bajor@upwr.edu.pl

Journal

Journal ID (nlm-ta): Virol J

Journal ID (iso-abbrev): Virol J

Title: Virology Journal

Publisher: BioMed Central (London )

ISSN (Electronic): 1743-422X

Publication date (Electronic): 8 September 2021

Publication date PMC-release: 8 September 2021

Publication date Collection: 2021

Volume: 18

Electronic Location Identifier: 183

Affiliations

[1 ]GRID grid.411200.6, ISNI 0000 0001 0694 6014, Department of Biotechnology and Food Microbiology, Faculty of Biotechnology and Food Sciences, , Wrocław University of Environmental and Life Sciences, ; Wrocław, Poland

[2 ]GRID grid.411200.6, ISNI 0000 0001 0694 6014, Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, , Wrocław University of Environmental and Life Sciences, ; Wrocław, Poland

[3 ]GRID grid.411200.6, ISNI 0000 0001 0694 6014, Department of Epizootiology and Clinic of Birds and Exotic Animals, Faculty of Veterinary Medicine, , Wrocław University of Environmental and Life Sciences, ; Wrocław, Poland

[4 ]GRID grid.8585.0, ISNI 0000 0001 2370 4076, Department of Electron Microscopy, Faculty of Biology, , University of Gdansk, ; Gdansk, Poland

Author information

Marta Kuźmińska-Bajor http://orcid.org/0000-0003-1904-1059

Article

Publisher ID: 1655

DOI: 10.1186/s12985-021-01655-4

PMC ID: 8425127

PubMed ID: 34496915

SO-VID: eb600add-7228-41d3-838d-7f0cc40a127d

License:

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/. The Creative Commons Public Domain Dedication waiver ( http://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.

History

Date received : 6 April 2021

Date accepted : 29 August 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100005632, Narodowe Centrum Badań i Rozwoju;

Award ID: LIDER/378/L-6/14/NCBR/2015

Award Recipient : Marta Kuźmińska-Bajor

Custom metadata

ScienceOpen disciplines: Microbiology & Virology

Keywords: salmonella enterica,bacteriophages,bacteriophage genetics,comparative genomics

Data availability:

ScienceOpen disciplines: Microbiology & Virology

Keywords: salmonella enterica, bacteriophages, bacteriophage genetics, comparative genomics

Genomic and functional characterization of five novel Salmonella-targeting bacteriophages

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