Abstract
Staphylococcus aureus is a significant pathogen associated with various illnesses, including food poisoning. The development of effective treatments is challenging, necessitating the exploration of novel antimicrobial options. Bacteriophages (phages) have emerged as promising candidates in this regard. In this study, a virulent phage called mSA4 was isolated and characterized. Furthermore, its efficacy in combating S. aureus biofilms and growth in various food products was evaluated. Phage mSA4 demonstrated a broad host range, targeting both S. aureus and methicillin-resistant S. aureus strains. Belonging to the Myoviridae family, it exhibited rapid adsorption (over 50% in 3 min), a short latent period (20 min), and a burst size of 97 phage particles per infected bacterial cell. Furthermore, phage mSA4 displayed stability across a wide range of pH values and temperatures, and effectively degraded established biofilms. Its performance was evaluated in chocolate milk, beef meat, and iceberg lettuce, resulting in significant reductions in bacterial counts (2.1 log CFU/mL, 2.8 log CFU/cm2, and 3.2 log CFU/cm2, respectively). These findings underscore the potential of phage mSA4 as a natural biocontrol agent against S. aureus.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alves DR, Gaudion A, Bean JE, Perez Esteban P, Arnot TC, Harper DR, Kot W, Hansen LH, Enright MC, Jenkins AT (2014) Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. Appl Environ Microbiol 80:6694–6703. https://doi.org/10.1128/AEM.01789-14
Chang Y, Bai J, Lee JH, Ryu S (2019) Mutation of a Staphylococcus aureus temperate bacteriophage to a virulent one and evaluation of its application. Food Microbiol 82:523–532. https://doi.org/10.1016/j.fm.2019.03.025
Duarte AC, Fernández L, De Maesschalck V, Gutiérrez D, Campelo AB, Briers Y, Lavigne R, Rodríguez A, García P (2021) Synergistic action of phage phiIPLA-RODI and lytic protein CHAPSH3b: a combination strategy to target Staphylococcus aureus biofilms. NPJ Biofilms Microbiomes 7:39. https://doi.org/10.1038/s41522-021-00208-5
Garvey M (2022) Bacteriophages and food production: biocontrol and bio-preservation options for food safety. Antibiotics (basel) 11:1324. https://doi.org/10.3390/antibiotics11101324
Gharieb RMA, Saad MF, Mohamed AS, Tartor YH (2020) Characterization of two novel lytic bacteriophages for reducing biofilms of zoonotic multidrug-resistant Staphylococcus aureus and controlling their growth in milk. LWT 124:109145. https://doi.org/10.1016/j.lwt.2020.109145
Korn AM, Hillhouse AE, Sun L, Gill JJ (2021) Comparative genomics of three novel jumbo bacteriophages infecting Staphylococcus aureus. J Virol 95:e0239120. https://doi.org/10.1128/JVI.02391-20
Kornienko M, Kuptsov N, Gorodnichev R, Bespiatykh D, Guliaev A, Letarova M, Kulikov E, Veselovsky V, Malakhova M, Letarov A, Ilina E, Shitikov E (2020) Contribution of Podoviridae and Myoviridae bacteriophages to the effectiveness of anti-staphylococcal therapeutic cocktails. Sci Rep 10:18612. https://doi.org/10.1038/s41598-020-75637-x
Leskinen K, Tuomala H, Wicklund A, Horsma-Heikkinen J, Kuusela P, Skurnik M, Kiljunen S (2017) Characterization of vB_SauM-fRuSau02, a twort-like bacteriophage isolated from a therapeutic phage cocktail. Viruses 9:258. https://doi.org/10.3390/v9090258
Lewis R, Hill C (2020) Overcoming barriers to phage application in food and feed. Curr Opin Biotechnol 61:38–44. https://doi.org/10.1016/j.copbio.2019.09.018
Mekhloufi OA, Chieffi D, Hammoudi A, Bensefia SA, Fanelli F, Fusco V (2021) Prevalence, enterotoxigenic potential and antimicrobial resistance of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) isolated from Algerian ready to eat foods. Toxins (basel) 13:835. https://doi.org/10.3390/toxins13120835
Moller AG, Winston K, Ji S, Wang J, Hargita Davis MN, Solís-Lemus CR, Read TD (2021) Genes influencing phage host range in Staphylococcus aureus on a species-wide scale. mSphere 6:e01263-e1320. https://doi.org/10.1128/mSphere.01263-20
Moye ZD, Woolston J, Sulakvelidze A (2018) Bacteriophage applications for food production and processing. Viruses 10:205. https://doi.org/10.3390/v10040205
Othman BR, Kuan CH, Mohammed AS, Cheah YK, Tan CW, New CY, Thung TY, Chang WS, Loo YY, Nakaguchi Y, Nishibuchi M, Radu S (2018) Occurrence of methicillin-resistant Staphylococcus aureus in raw shellfish at retail markets in Malaysia and antibacterial efficacies of black seed (Nigella sativa) oil against MRSA. Food Control 90:324–331. https://doi.org/10.1016/j.foodcont.2018.02.045
Saber T, Samir M, El-Mekkawy RM, Ariny E, El-Sayed SR, Enan G, Abdelatif SH, Askora A, Merwad AMA, Tartor YH (2022) Methicillin- and vancomycin-resistant Staphylococcus aureus from humans and ready-to-eat meat: characterization of antimicrobial resistance and biofilm formation ability. Front Microbiol 12:735494. https://doi.org/10.3389/fmicb.2021.735494
Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Shimamori Y, Pramono AK, Kitao T, Suzuki T, Aizawa SI, Kubori T, Nagai H, Takeda S, Ando H (2021) Isolation and characterization of a novel phage SaGU1 that infects Staphylococcus aureus clinical isolates from patients with atopic dermatitis. Curr Microbiol 78:1267–1276. https://doi.org/10.1007/s00284-021-02395-y
Song J, Ruan H, Chen L, Jin Y, Zheng J, Wu R, Sun D (2021) Potential of bacteriophages as disinfectants to control of Staphylococcus aureus biofilms. BMC Microbiol 21:57. https://doi.org/10.1186/s12866-021-02117-1
Tan CW, Rukayadi Y, Hasan H, Abdul-Mutalib NA, Jambari NN, Hara H, Thung TY, Lee E, Radu S (2021) Isolation and characterization of six Vibrio parahaemolyticus lytic bacteriophages from seafood samples. Front Microbiol 12:616548. https://doi.org/10.3389/fmicb.2021.616548
Thung TY, Lee E, Mahyudin NA, Anuradha K, Mazlan N, Kuan CH, Pui CF, Ghazali FM, Rashid NKMA, Rollon WD, Tan CW, Radu S (2019) Evaluation of a lytic bacteriophage for bio-control of Salmonella Typhimurium in different food matrices. LWT 105:211–214. https://doi.org/10.1016/j.lwt.2019.02.033
Acknowledgements
This research was funded by the grant from Fundamental Research Grant Scheme (FRGS) of the Ministry of Higher Education (MOHE), Malaysia (FRGS/1/2019/STG05/UNIMAS/03/2).
Author information
Authors and Affiliations
Contributions
FL and DL conducted the biological experiments. NM and EN performed the statistical analysis and wrote the draft. TYT conceptualized the idea and performed the final review of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lambuk, F., Mazlan, N., Lesen, D. et al. Staphylococcus aureus lytic bacteriophage: isolation and application evaluation. J Consum Prot Food Saf (2024). https://doi.org/10.1007/s00003-024-01479-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00003-024-01479-8