Abstract
Some serovars of Salmonella can cause life-threatening diarrhoeal diseases and bacteriemia. The emergence of multidrug-resistant strains has led to a need for alternative treatments such as phage therapy, which requires available, well-described, diverse, and suitable phages. Phage akira was found to lyse 19 out of 32 Salmonella enterica serovars and farm isolates tested, although plaque formation was observed with only two S. Enteritidis and one S. Typhimurium strain. Phage akira encodes anti-defence genes against type 1 R-M systems, is distinct (<65% nucleotide sequence identity) from related phages and has siphovirus morphology. We propose that akira represents a new genus in the class Caudoviricetes.
Availability of data and material
The genome sequence of Salmonella phage akira is available in the GenBank database under the accession number NC_054647.1. All data generated or analysed during this study are included in this published article and its supplementary files.
References
World health Organization (WHO) (2008) Salmonella (non-typhoidal). https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal). Accessed 6 Sep 2021
Middleton D, Savage R, Tighe MK et al (2014) Risk factors for sporadic domestically acquired Salmonella serovar Enteritidis infections: a case-control study in Ontario, Canada, 2011. Epidemiol Infect 142:1411–1421. https://doi.org/10.1017/S0950268813001945
Much P, Pichler J, Kasper S et al (2009) A foodborne outbreak of Salmonella enteritidis phage type 6 in Austria, 2008. Wien Klin Wochenschr 121:132–136. https://doi.org/10.1007/s00508-008-1134-y
European Food Safety Authority (2021) The European Union One Health 2019 Zoonoses Report
Shrivastava SR, Shrivastava PS, Ramasamy J (2018) World health organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. JMS - J Med Soc 32:76–77. https://doi.org/10.4103/jms.jms_25_17
Koutsoumanis K, Allende A, Álvarez-Ordóñez A, et al (2021) Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain
Khatami A, Lin RCY, Petrovic-Fabijan A et al (2021) Bacterial lysis, autophagy and innate immune responses during adjunctive phage therapy in a child. EMBO Mol Med 13:e13936. https://doi.org/10.15252/emmm.202113936
Hatfull GF, Dedrick RM, Schooley RT (2022) Phage therapy for antibiotic-resistant bacterial infections. Annu Rev Med. https://doi.org/10.1146/annurev-med-080219-122208
Kwiatek M, Parasion S, Nakonieczna A (2020) Therapeutic bacteriophages as a rescue treatment for drug-resistant infections—an in vivo studies overview. J Appl Microbiol 128:985–1002. https://doi.org/10.1111/jam.14535
Capparelli R, Nocerino N, Lannaccone M et al (2010) Bacteriophage therapy of Salmonella enterica: a fresh appraisal of bacteriophage therapy. J Infect Dis 201:52–61. https://doi.org/10.1086/648478
Cook R, Brown N, Redgwell T et al (2021) INfrastructure for a PHAge REference database: identification of large-scale biases in the current collection of cultured phage genomes. Phage 2:214–223. https://doi.org/10.1089/phage.2021.0007
Turner D, Kropinski AM, Adriaenssens EM (2021) A roadmap for genome-based phage taxonomy. Viruses. https://doi.org/10.3390/v13030506
Olsen NS, Hendriksen NB, Hansen LH, Kot W (2020) A New High-throughput Screening (HiTS) Method for Phages—enabling crude isolation and fast identification of diverse phages with therapeutic potential. PHAGE. https://doi.org/10.1101/2020.03.27.011080
Brettin T, Davis JJ, Disz T et al (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365. https://doi.org/10.1038/srep08365
Besemer J, Lomsadze A, Borodovsky M (2001) GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. 29:2607–2618. https://doi.org/10.1093/nar/29.12.2607
Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Hildebrand A, Remmert M, Biegert A, Söding J (2009) Fast and accurate automatic structure prediction with HHpred. Proteins Struct Funct Bioinf 77:128–132. https://doi.org/10.1002/prot.22499
Zankari E, Hasman H, Cosentino S et al (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644. https://doi.org/10.1093/jac/dks261
Meier-Kolthoff JP, Göker M (2017) VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics 33:3396–3404. https://doi.org/10.1093/bioinformatics/btx440
Moraru C, Varsani A, Kropinski AM (2020) VIRIDIC—a novel tool to calculate the intergenomic similarities of prokaryote-infecting viruses. Viruses 12:1268. https://doi.org/10.3390/v12111268
Gilchrist CLM, Chooi Y-H (2021) clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 37:2473–2475. https://doi.org/10.1093/bioinformatics/btab007
Letarov A V., Kulikov EE (2018) Determination of the bacteriophage host range: Culture-Based approach. In: Methods in Molecular Biology. Humana Press Inc., pp 75–84
Zhang R, Mirdita M, Levy Karin E et al (2021) SpacePHARER: sensitive identification of phages from CRISPR spacers in prokaryotic hosts. Bioinformatics. https://doi.org/10.1093/bioinformatics/btab222
Dion MB, Plante PL, Zufferey E et al (2021) Streamlining CRISPR spacer-based bacterial host predictions to decipher the viral dark matter. Nucleic Acids Res 49:3127–3138. https://doi.org/10.1093/nar/gkab133
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press
Sullivan M (2016) Cesium chloride dialysis for viruses. https://doi.org/10.17504/protocols.io.c7jzkm
Lavelle K, Martinez I, Neve H et al (2018) Biodiversity of streptococcus thermophilus phages in global dairy fermentations. Viruses 10:577. https://doi.org/10.3390/v10100577
Carstens AB, Kot W, Lametsch R et al (2016) Characterisation of a novel enterobacteria phage, CAjan, isolated from rat faeces. Arch Virol 161:2219–2226. https://doi.org/10.1007/s00705-016-2901-0
King G, Murray NE (1995) Restriction alleviation and modification enhancement by the Rac prophage of Escherichia coli K-12. Mol Microbiol 16:769–777. https://doi.org/10.1111/j.1365-2958.1995.tb02438.x
Lu MJ, Henning U (1989) The immunity (imm) gene of Escherichia coli bacteriophage T4. J Virol 63:3472–3478. https://doi.org/10.1128/jvi.63.8.3472-3478.1989
Sui B, Qi X, Wang X et al (2021) Characterization of a novel bacteriophage swi2 harboring two lysins can naturally lyse Escherichia coli. Front Microbiol 12:1201. https://doi.org/10.3389/fmicb.2021.670799
Rohren M, Xie Y, O’Leary C et al (2019) Complete genome sequence of Salmonella enterica Serovar Typhimurium Siphophage Skate. Microbiol Resour Announc 8:e00541-e619. https://doi.org/10.1128/mra.00541-19
Choi IY, Lee C, Song WK et al (2019) Lytic KFS-SE2 phage as a novel bio-receptor for Salmonella enteritidis detection. J Microbiol 57:170–179
Huang C, Shi J, Ma W et al (2018) Isolation, characterization, and application of a novel specific Salmonella bacteriophage in different food matrices. Food Res Int 111:631–641. https://doi.org/10.1016/j.foodres.2018.05.071
Doore SM, Schrad JR, Dean WF et al (2018) Shigella phages isolated during a dysentery outbreak reveal uncommon structures and broad species Diversity. J Virol. https://doi.org/10.1128/jvi.02117-17
Turner D, Adriaenssens EM, Tolstoy I, Kropinski AM (2021) Phage annotation guide: guidelines for assembly and high-quality annotation. Phage 2:170–182. https://doi.org/10.1089/phage.2021.0013
Stoddard BL (2011) Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure 19:7–15
Goodrich-Blair H, Shub DA (1996) Beyond homing: competition between intron endonucleases confers a selective advantage on flanking genetic markers. Cell 84:211–221. https://doi.org/10.1016/S0092-8674(00)80976-9
Kala S, Cumby N, Sadowski PD et al (2014) HNH proteins are a widespread component of phage DNA packaging machines. Proc Natl Acad Sci USA 111:6022–6027. https://doi.org/10.1073/pnas.1320952111
Hampton HG, Watson BNJ, Fineran PC (2020) The arms race between bacteria and their phage foes. Nature 577:327–336. https://doi.org/10.1038/s41586-019-1894-8
Abedon ST (2011) Lysis from without. Bacteriophage 1:46–49. https://doi.org/10.4161/bact.1.1.13980
Liu Y, Mi L, Mi Z et al (2016) Complete genome sequence of IME207, a novel bacteriophage which can lyse multidrug-resistant Klebsiella pneumoniae and Salmonella. Genome Announc 4:2015–2016. https://doi.org/10.1128/genomeA.01015-16
Guo Y, Li J, Islam MS et al (2021) Application of a novel phage vB_SalS-LPSTLL for the biological control of Salmonella in foods. Food Res Int 147:110492. https://doi.org/10.1016/j.foodres.2021.110492
Anwar MZ, Zervas A, Hansen LH et al (2020) Complete genome and plasmid sequences of Salmonella enterica subsp. enterica Serovar Enteritidis PT1, obtained from the Salmonella Reference Laboratory at Public Health England, Colindale, United Kingdom. Microbiol Resour Announc. https://doi.org/10.1128/mra.01064-19
Acknowledgements
The authors are grateful to Herning Vand (DANVA) for the wastewater sample, the Danish Veterinary and Food Administration for providing the Salmonella strains, and Laura Forero-Junco (KU, DK) for help with SpacePHARER.
Funding
This research was funded by Villum Experiment Grant 17595, Aarhus University Research Foundation AUFF Grant E-2015-FLS-7-28 (Witold Kot), and Human Frontier Science Program Grant RGP0024/2018 (Lars H. Hansen).
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NSO, LHH, and WK contributed to the study conception and design. Material preparation, data collection, and analysis were performed by NSO, RL, and NW. The first draft of the manuscript was written by NSO, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Olsen, N.S., Lametsch, R., Wagner, N. et al. Salmonella phage akira, infecting selected Salmonella enterica Enteritidis and Typhimurium strains, represents a new lineage of bacteriophages. Arch Virol 167, 2049–2056 (2022). https://doi.org/10.1007/s00705-022-05477-9
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DOI: https://doi.org/10.1007/s00705-022-05477-9