In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage

Hilal Basak Erol; Banu Kaşkatepe

In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage

Abstract

Salmonella is an important agent that causes foodborne gastrointestinal infections. Salmonella enterica serovar Enteritidis, serovar Typhimurium, and serovar Infantis are the main pathogenic agents of several enteric infections worldwide. Due to the emergence of multidrug resistant Salmonella strains, there is a need for new administration strategies alternative to antibiotics, such as bacteriophages, for effective control of them. The main objectives of this study were to isolate and characterize Salmonella spp. bacteriophage and compare its activity to commercial phage product and assess the effect of bacteriophages in vitro during 24-h. Because of the study, it was found that the newly isolated and named vB_SiM_12 phage could lyse 100% of the strains tested. Bacterial growth with dilutions of vB_SiM_12 phage (MOI ranging from 0.001 to 10) was measured during 24-h. The optic density values of the samples with added bacteriophage remained lower than the control sample during the 24-h incubation period. The results show that using phages may offer a promising alternative to combat biological control agents against Salmonella infection.

Keywords

References

[1] Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH. Salmonella: A review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci. 2015; 8(3): 284-293. https://doi.org/10.1080/21553769.2015.1051243
[2] Tauxe RV. Emerging foodborne diseases: an evolving public health challenge. Emerg Infect Dis. 1997; 3(4): 425-434. https://doi.org/10.3201/eid0304.970403
[3] Carrasco E, Morales-Rueda A, García-Gimeno RM. Cross-contamination and recontamination by Salmonella in foods: A review. Food Res Int. 2012; 45(2): 545-556. https://doi.org/10.1016/j.foodres.2011.11.004
[4] Parry CM, Beeching NJ. Epidemiology, diagnosis and treatment of enteric fever. Curr Opin Infect Dis. 1998; 11(5): 583-590.
[5] Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis: The role of poultry meat. Clin Microbiol Infect. 2016; 22(2): 110-121. https://doi.org/10.1016/j.cmi.2015.12.004
[6] ChenHM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella Infection: Microbiology, clinical features, and antimicrobial therapy. Pediatr Neonatol. 2013; 54(3): 147-152. https://doi.org/10.1016/j.pedneo.2013.01.010
[7] Noto Llana M, Sarnacki SH, Aya Castañeda MDR, Pustovrh MC, Gartner AS, Buzzola FR, Giacomodonato MN. Salmonella enterica Serovar Enteritidis Enterocolitis during late stages of gestation induces an adverse pregnancy outcome in the murine model. PLoS One. 2014; 9(11): e111282.https://doi.org/10.1371/journal.pone.0111282
[8] European Food Safety, A, European Centre for Disease, P, Control. The European Union One Health 2018 ZoonosesReport. EFSA journal. European Food Safety Authority. 2019; 17(12): e05926. https://doi.org/10.2903/j.efsa.2019.5926

[9] Gonzalez-Escobedo G, Gunn JS. Gallbladder epithelium as a niche for chronic Salmonella carriage. Infect Immun. 2013; 81(8): 2920-2930. https://doi.org/10.1128/iai.00258-13
[10] Esmaeil Zadeh MR, Sharifi Yazdi MK, Rajabi Z, Amin Harati F, Nikkhahi F, Sharifi Yazdi S, SoltanDallal MM. Evaluation of specific bacteriophage against SalmonellaInfantis and its antibacterial effects compared to ciprofloxacin in in vitro conditions. J Adv Med Biomed Res. 2022; 30(139): 154-161.
[11] Thung TY, Premarathne JMKJK, San Chang W, Loo YY, Chin, YZ, Kuan CH, Radu S. Use of a lytic bacteriophage to control Salmonella Enteritidis in retail food. LWT. 2017; 78: 222-225. https://doi.org/10.1016/j.lwt.2016.12.044
[12] García P, Martínez B, Obeso JM, Rodríguez A. Bacteriophages and their application in food safety. Lett Appl Microbiol. 2008; 47(6): 479-485. https://doi.org/10.1111/j.1472-765X.2008.02458.x
[13] Wittebole X, De Roock S, Opal SM. A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence. 2014; 5(1): 226-235 . https://doi.org/10.4161%2Fviru.25991.
[14] Carlton RM, Noordman WH, Biswas B, de Meester ED, Loessner MJ. Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul Toxicol Pharmacol. 2005; 43(3): 301-312. https://doi.org/10.1016/j.yrtph.2005.08.005
[15] Moye ZD, Woolston J, Sulakvelidze A. Bacteriophage Applications for Food Production and Processing. Viruses. 2018; 10(4):205. https://doi:10.3390/v10040205
[16] Barrow PA, Jones MA, Smith AL, Wigley P. The long view: Salmonella – the last forty years. Avian Pathol. 2012; 41(5): 413-420. https://doi.org/10.1080/03079457.2012.718071
[17] Center for Disease Control and Prevention. Salmonella. Available online: https://www.cdc.gov/salmonella/index.html (accessed on 20 November 2022).
[18] Petsong K, Benjakul S, Chaturongakul S, Switt AIM, Vongkamjan K. Lysis profiles of Salmonella phages on Salmonella isolates from various sources and efficiency of a phage cocktail against S. enteritidis and S. typhimurium. Microorganisms. 2019; 7(4): 100. https://doi.org/10.3390/microorganisms7040100
[19] Cummings KJ,Warnick LD, Alexander KA, Cripps CJ,Gröhn YT, James KL, McDonough PL, Reed KE. The duration of fecal Salmonella shedding following clinical disease among dairy cattle in the northeastern USA. Prev Vet Med. 2009; 92: 134–139. https://doi.org/10.1016/j.prevetmed.2009.07.002
[20] Moreno Switt AI, den Bakker HC,Vongkamjan K,Hoelzer K,Warnick LD, Cummings KJ, Wiedmann M. Salmonella bacteriophage diversity reflects host diversity on dairy farms. Food Microbiol. 2013; 36: 275–285. https://doi.org/10.1016/j.fm.2013.06.014
[21] Sun F, Li X, Wang Y, Wang F, Ge H, Pan Z, Xu Y, Wang Y, Jiao X, Chen X. Epidemic patterns of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century. Poult Sci. 2021; 100: 100894.https://doi.org/10.1016/j.psj.2020.12.007
[22] Eriksson H, Soderlund R, Ernholm L, Melin L, Jansson DS. Diagnostics, epidemiological observations and genomic subtyping in an outbreak of pullorum disease in non-commercial chickens. Vet Microbiol. 2018; 217: 47–52. https://doi.org/10.1016/j.vetmic.2018.02.025
[23] Kumari S, Harjai K, Chhibber S. Bacteriophage versus antimicrobial agents for the treatment of murine burn wound infection caused by Klebsiella pneumoniae B5055. J Med Microbiol.2011; 60(2): 205-210. https://doi.org/10.1099/jmm.0.018580-0
[24] Oliveira H, Sillankorva S, Merabishvili M, Kluskens LD, AzeredoJ. Unexploited opportunities for phage therapy. Front Pharmacol. 2015; 6: 180. https://doi.org/10.3389/fphar.2015.00180.
[25] Iversen C, Mullane N, McCardell B, Tall BD, Lehner A, Fanning S, Stephan R, Joosten H. Cronobactergen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobactersakazakii gen. nov., comb. nov., Cronobactermalonaticus sp. nov., Cronobacterturicensis sp. nov., Cronobactermuytjensii sp. nov., Cronobacterdublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, Cronobacterdublinensis subsp. dublinensis subsp. nov., Cronobacterdublinensis subsp. lausannensis subsp. nov. and Cronobacterdublinensis subsp. lactaridi subsp. nov. Int J Syst Evol Microbiol. 2008; 58: 1442–1447. https://doi.org/10.1099/ijs.0.65577-0
[26] Adeolu M, Alnajar S, Naushad S, Gupta RS. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: Proposal for enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol. 2016; 66: 5575–5599. https://doi.org/10.1099/ijsem.0.001485
[27] Gencay YE, Gambino M, Prüssing TF, Brøndsted L. The genera of bacteriophages and their receptors are the major determinants of host range. Environ Microbiol. 2019; 21(6): 2095-2111. https://doi.org/10.1111/1462-2920.14597
[28] Choi IY, Lee JH, Kim HJ, Park MK. Isolation and characterization of a novel broad-host-range bacteriophage infecting Salmonella enterica subsp. enterica for biocontrol and rapid detection. J Microbiol Biotechnol. 2017; 27: 2151–2155. https://doi.org/10.4014/jmb.1711.11017
[29] Huang C, Shi J, Ma W, Li Z, Wang J, Li J, WangX. Isolation, characterization, and application of a novel specific salmonella bacteriophage in different food matrices. Food Res Int. 2018; 111: 631–641. https://doi.org/10.1016/j.foodres.2018.05.071
[30] Bao H, Zhang P, Zhang H, Zhou Y, Zhang L, Wang R. Biocontrol of Salmonella enteritidis in Foods Using Bacteriophages. Viruses. 2015; 7(8): 4836–4853. https://doi.org/10.3390/v7082847
[31] Ge H, Lin C, Xu Y, Hu M, Xu Z, Geng S, Chen X. A phage for the controlling of Salmonella in poultry and reducing biofilms. Vet Microbiol. 2022; 269, 109432. https://doi.org/10.1016/j.vetmic.2022.109432
[32] Wernicki A,Nowaczek R, Urban-Chmiel R. Bacteriophage therapy to combat bacterial infections in poultry.Virol J. 2017; 14: 179. https://doi.org/10.1186%2Fs12985-017-0849-7
[33] Carvalho CM, Gannon BW, Halfhide DE, Santos SB, Hayes CM, Roe JM,Azeredo J. The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiol. 2010; 10: 1-11. https://doi.org/10.1186/1471-2180-10-232
[34] Leshkasheli L, Kutateladze M, Balarjishvili N, Bolkvadze D, Save J, Oechslin F, Resch G. Efficacy of newly isolated and highly potent bacteriophages in a mouse model of extensively drug-resistant Acinetobacter baumannii bacteraemia. J Glob Antimicrob Resist. 2019; 19: 255-261. https://doi.org/10.1016/j.jgar.2019.05.005
[35] Sevilla-Navarro S, Catalá-Gregori P, García C, Cortés V,Marin C. Salmonella infantis and Salmonella enteritidis specific bacteriophages isolated form poultry faeces as a complementary tool for cleaning and disinfection against Salmonella. Comp Immunol Microbiol Infect Dis. 2020; 68, 101405. https://doi.org/10.1016/j.cimid.2019.101405
[36] Imklin N, Nasanit R. Characterization of Salmonella bacteriophages and their potential use in dishwashing materials. J Appl Microbiol. 2020; 129(2): 266-277. https://doi.org/10.1111/jam.14617
[37] Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP. Enumeration of bacteriophages by double agar overlay plaque assay. Methods Mol Biol (Clifton, NJ). 2009; 501:69-76. https://doi.org/10.1007/978-1-60327-164-6_7
[38] Adams MH. Bacteriophages: Interscience publishers; 1959.
[39] Merabishvili M, Pirnay J-P, Verbeken G, Chanishvili N, Tediashvili M, Lashkhi N, Glonti T, Krylov V, Mast J, Parys LV, Lavigne R, Volckaert G, Mattheus W, Verween G, De Corte P, Rose T, Jennes S, Zizi M, De Vos D, Vaneechoutte M. Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PloS one. 2009; 4(3): 4944-4955. https://doi.org/10.1371/journal.pone.0004944
[40] Oliveira H, Pinto G, Oliveira A, Oliveira C, Faustino MA, Briers Y, Domingues L, Azeredo J. Characterization and genome sequencing of a Citrobacter freundii phage CfP1 harboring a lysin active against multidrug-resistant isolates. Appl Microbiol Biotechnol. 2016; 100(24): 10543-10553. https://doi.org/10.1007/s00253-016-7858-0.
[41] Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: A laboratory manual: Cold spring harbor laboratory press; 1989.
[42] Sasikala D, Srinivasan P. Characterization of potential lytic bacteriophage against Vibrio alginolyticus and its therapeutic implications on biofilm dispersal. Microb Pathog. 2016; 101: 24-35. https://doi.org/10.1016/j.micpath.2016.10.017
[43] Ackermann HW. Basic phage electron microscopy. Methods Mol Biol. 2009; 501: 113-126. https://doi.org/10.1007/978-1-60327-164-6_12

Details

Primary Language

English

Subjects

Pharmaceutical Microbiology

Journal Section

Research Article

Authors

Hilal Basak Erol ^*
0000-0002-7943-755X
Türkiye

Banu Kaşkatepe
0000-0002-9722-4267
Türkiye

Publication Date

June 28, 2025

Submission Date

March 31, 2023

Acceptance Date

July 4, 2023

Published in Issue

Year 2024 Volume: 28 Number: 1

IZ

https://izlik.org/JA46ET82YF

Cite

RIS / Bibtex

APA

Erol, H. B., & Kaşkatepe, B. (2025). In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage. Journal of Research in Pharmacy, 28(1), 133-141. https://izlik.org/JA46ET82YF

AMA

1.Erol HB, Kaşkatepe B. In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage. J. Res. Pharm. 2025;28(1):133-141. https://izlik.org/JA46ET82YF

Chicago

Erol, Hilal Basak, and Banu Kaşkatepe. 2025. “In Vitro Bacteriolytic Activity of Salmonella Specific Novel Isolated Bacteriophage”. Journal of Research in Pharmacy 28 (1): 133-41. https://izlik.org/JA46ET82YF.

EndNote

Erol HB, Kaşkatepe B (June 1, 2025) In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage. Journal of Research in Pharmacy 28 1 133–141.

IEEE

[1]H. B. Erol and B. Kaşkatepe, “In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage”, J. Res. Pharm., vol. 28, no. 1, pp. 133–141, June 2025, [Online]. Available: https://izlik.org/JA46ET82YF

ISNAD

Erol, Hilal Basak - Kaşkatepe, Banu. “In Vitro Bacteriolytic Activity of Salmonella Specific Novel Isolated Bacteriophage”. Journal of Research in Pharmacy 28/1 (June 1, 2025): 133-141. https://izlik.org/JA46ET82YF.

JAMA

1.Erol HB, Kaşkatepe B. In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage. J. Res. Pharm. 2025;28:133–141.

MLA

Erol, Hilal Basak, and Banu Kaşkatepe. “In Vitro Bacteriolytic Activity of Salmonella Specific Novel Isolated Bacteriophage”. Journal of Research in Pharmacy, vol. 28, no. 1, June 2025, pp. 133-41, https://izlik.org/JA46ET82YF.

Vancouver

1.Hilal Basak Erol, Banu Kaşkatepe. In vitro bacteriolytic activity of Salmonella specific novel isolated bacteriophage. J. Res. Pharm. [Internet]. 2025 Jun. 1;28(1):133-41. Available from: https://izlik.org/JA46ET82YF