Isolation and characterization of a broad-spectrum phage SapYZU11 and its potential application for biological control of Staphylococcus aureus
Main Article Content
Keywords
bacteriophage, biocontrol, food security, milk, Staphylococcus aureus
Abstract
Staphylococcus aureus, a prominent pathogen, is frequently encountered in clinical and food-processing settings. Given its ability to develop antimicrobial resistance, effective control strategies are required to ensure microbial safety. In this study, four lytic S. aureus phages (SapYZU10, SapYZU11, SapYZU12, and SapYZU13) were isolated from sewage samples in Yangzhou, China. Their biological characteristics and bactericidal effect against S. aureus isolates in vitro and in milk and fresh pork were evaluated. Their activities remained relatively stable under stressful conditions (-80–70°C, pH 3.0–12.0). Notably, SapYZU11 (100%, 53/53) effectively lysed all 53 S. aureus strains, followed by SapYZU12 (90.57%, 48/53), SapYZU13 (79.25%, 42/53), and SapYZU10 (71.70%, 38/53). Among the phages with short latent periods (10–20 min), SapYZU11 had a larger burst size (152.00 plaque forming units [PFU]/mL) and no genes related to antibiotic resistance and virulence. Furthermore, SapYZU11 effectively eradicated S. aureus and its cocktail (YZUsa1, YZUsa4, YZUsa12, YZUsa14, and methicillin-resistance S. aureus (MRSA) JCSC 4744) in Luria–Bertani broth and both food items. Particularly in milk, SapYZU11 with a multiplicity of infection (MOI) of 100 inhibited MRSA JCSC 4744 strain and S. aureus cocktail with maximum reduction levels of 5.03 log (Lg) colony-forming unit (CFU)/mL and 2.80 Lg CFU/mL, respectively. Conversely, contaminated pork treated with three MOIs of SapYZU11 at 25°C and 4°C resulted in reductions of 0.29–1.29 Lg CFU/mL and 0.11–0.32 Lg CFU/mL, respectively. Therefore, SapYZU11 proved as a promising biocontrol agent against S. aureus in different food production settings.
References
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Li, H., Yang, X., Zhu, X., Gao, L., Rao, S., Yuan, L., et al. 2021a. Isolation and characterization of broad host-range of bacteriophages infecting Cronobacter sakazakii and its biocontrol potential in dairy products. Quality Assurance and Safety of Crops & Foods 13: 21–44. 10.15586/QAS.V13I3.890
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Meaden, S. and Koskella, B., 2013. Exploring the risks of phage application in the environment. Frontiers in Microbiology 4: 358. 10.3389/fmicb.2013.00358
Miedzybrodzki, R., Borysowski, J., Weber-Dabrowska, B., Fortuna, W., Letkiewicz, S., Szufnarowski, K., et al. 2012. Clinical aspects of phage therapy. Advances in Virus Research 83: 73–121. 10.1016/B978-0-12-394438-2.00003-7
Monteiro, R., Pires, D.P., Costa, A.R. and Azeredo, J., 2019. Phage therapy: going temperate? Trends in Microbiology 27: 368–378. 10.1016/j.tim.2018.10.008
Nikolic, P., Mudgil, P. and Whitehall, J., 2020. The in vitro antibacterial effect of permethrin and formaldehyde on Staphylococcus aureus. MicrobiologyOpen 9: e1054. 10.1002/mbo3.1054
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Witte, S., Huijboom, L., Klamert, S., van de Straat, L., Hagens, S., Fieseler, L., et al. 2022. Application of bacteriophages EP75 and EP335 efficiently reduces viable cell counts of Escherichia coli O157 on beef and vegetables. Food Microbiology 104: 103978. 10.1016/j.fm.2022.103978
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Zhang, L., Shahin, K., Soleimani-Delfan, A., Ding, H., Wang, H., Sun, L., et al. 2022b. Phage JS02, a putative temperate phage, a novel biofilm-degrading agent for Staphylococcus aureus. Letters in Applied Microbiology 75: 643–654. 10.1111/lam.13663
Zhang, F., Wu, S., Lei, T., Wu, Q., Zhang, J., Huang, J., et al. 2022a. Presence and characterization of methicillin-resistant Staphylococcus aureus co-carrying the multidrug resistance genes cfr and lsa (E) in retail food in China. International Journal of Food Microbiology 363: 109512. 10.1016/j.ijfoodmicro.2021.109512
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Zhou, W.Y., Li, X., Osmundson, T., Shi, L., Ren, J. and Yan, H., 2018a. WGS analysis of ST9-MRSA-XII isolates from live pigs in China provides insights into transmission among porcine, human and bovine hosts. Journal of Antimicrobial Chemotherapy 73: 2652–2661. 10.1093/jac/dky245
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Zhou, W.Y., Sun, S.F., Zhang, Y.S., Hu, Q., Zheng, X.F., Yang, Z.Q., et al. 2021. Isolation and characterization of a virulent bacteriophage for controlling Salmonella Enteritidis growth in ready-to-eat nixed-ingredient salads. Journal of Food Protection 84: 1629–1639. 10.4315/JFP-20-460
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Alves, D.R., Gaudion, A., Bean, J.E., Perez, E.P., Arnot, T.C., Harper, D.R., et al. 2014. Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. Applied and Environmental Microbiology 80: 6694–6703. 10.1128/AEM.01789-14
Amarillas, L., Rubi-Rangel, L., Chaidez, C., Gonzalez-Robles, A., Lightbourn-Rojas, L. and Leon-Felix, J., 2017. Isolation and characterization of phiLLS, a novel phage with potential biocontrol agent against multidrug-resistant Escherichia coli. Frontiers in Microbiology 8: 1355. 10.3389/fmicb.2017.01355
Bhetwal, A., Maharjan, A., Shakya, S., Satyal, D., Ghimire, S., Khanal, P.R. et al. 2017. Isolation of potential phages against multidrug-resistant bacterial isolates: promising agents in the rivers of Kathmandu, Nepal. BioMed Research International 2017: 3723254. 10.1155/2017/3723254
Cao, Y., Zhang, Y., Lan, W. and Sun, X., 2021. Characterization of vB_VpaP_MGD2, a newly isolated bacteriophage with biocontrol potential against multidrug-resistant Vibrio parahaemolyticus. Archives of Virology 166: 413–426. 10.1007/s00705-020-04887-x
Cha, Y., Chun, J., Son, B. and Ryu, S., 2019. Characterization and genome analysis of Staphylococcus aureus Podovirus CSA13 and its anti-biofilm capacity. Viruses (Basel) 11(1): 54. 10.3390/v11010054
Duc, H.M., Son, H.M., Yi, H., Sato, J., Ngan, P.H., Masuda, Y., et al. 2020. Isolation, characterization and application of a polyvalent phage capable of controlling Salmonella and Escherichia coli O157:H7 in different food matrices. Food Research International 131: 108977. 10.1016/j.foodres.2020.108977
Esmael, A., Azab, E., Gobouri, A.A., Nasr-Eldin, M.A., Moustafa, M., Mohamed, S.A., e al. 2021. Isolation and characterization of two lytic bacteriophages infecting a multi-drug resistant Salmonella Typhimurium and their efficacy to combat salmonellosis in ready-to-use foods. Microorganisms 9(2): 423. 10.3390/microorganisms9020423
Feng, T., Leptihn, S., Dong, K., Loh, B., Zhang, Y., Stefan, M.I., et al. 2021. JD419, a Staphylococcus aureus phage with a unique morphology and broad host range. Frontiers in Microbiology 12: 602902. 10.3389/fmicb.2021.602902
Gharieb, R.M.A., Saad, M.F., Mohamed, A.S. and Tartor, Y.H., 2020. Characterization of two novel lytic bacteriophages for reducing biofilms of zoonotic multidrug-resistant Staphylococcus aureus and controlling their growth in milk. Food Science and Technology (LWT) 124: 109145. 10.1016/j.lwt.2020.109145
Guo, Y., Li, J., Islam, M.S., Yan, T., Zhou, Y., Liang, L., et al. 2021. Application of a novel phage vB_SalS-LPSTLL for the biological control of Salmonella in foods. Food Research International 147: 110492. 10.1016/j.foodres.2021.110492
Iyer, K.R., Revie, N.M., Fu, C., Robbins, N. and Cowen, L.E., 2021. Treatment strategies for cryptococcal infection: challenges, advances and future outlook. Nature Reviews Microbiology 19: 454–466. 10.1038/s41579-021-00511-0
Kitamura, N., Sasabe, E., Matsuzaki, S., Daibata, M. and Yamamoto, T., 2020. Characterization of two newly isolated Staphylococcus aureus bacteriophages from Japan belonging to the genus Silviavirus. Archives of Virology 165: 2355–2359. 10.1007/s00705-020-04749-6
Kwon, J., Kim, S.G., Kim, H.J., Giri, S.S., Kim, S.W., Lee, S.B., et al. 2020. Isolation and characterization of Salmonella jumbo-phage pSal-SNUABM-04. Viruses (Basel) 13(1): 27. 10.3390/v13010027
Lewis, R. and Hill, C., 2020. Overcoming barriers to phage application in food and feed. Current Opinion in Biotechnology 61: 38–44. 10.1016/j.copbio.2019.09.018
Li, Y., Chen, H., Shu, M., Zhong, C., Bi, Y., Yang, H., et al. 2021b. Isolation, characterization and application of an alkaline resistant virulent bacteriophage JN01 against Escherichia coli O157:H7 in milk and beef. Food Science and Technology (LWT) 144: 111266. 10.1016/j.lwt.2021.111266
Li, G., Wu, C., Wang, X. and Meng, J., 2015. Prevalence and characterization of methicillin susceptible Staphylococcus aureus ST398 isolates from retail foods. International Journal of Food Microbiology 196: 94–97. 10.1016/j.ijfoodmicro.2014.12.002
Li, H., Yang, X., Zhu, X., Gao, L., Rao, S., Yuan, L., et al. 2021a. Isolation and characterization of broad host-range of bacteriophages infecting Cronobacter sakazakii and its biocontrol potential in dairy products. Quality Assurance and Safety of Crops & Foods 13: 21–44. 10.15586/QAS.V13I3.890
Luo, D., Li, C., Wu, Q., Ding, Y., Yang, M., Hu, Y., et al. 2021. Isolation and characterization of new phage vB_CtuP_A24 and application to control Cronobacter spp. in infant milk formula and lettuce. Food Research International 141: 110109. 10.1016/j.foodres.2021.110109
Ma, F., Ning, Y., Wan, Q., Zou, L., Liu, Y., Chen, S., et al. 2021. Bacteriophages LSA2308 and LSA2366 infecting drug-resistant Staphylococcus aureus: isolation, characterization and potential application for milk safety. Food Science and Technology (LWT) 152: 112298. 10.1016/j.lwt.2021.112298
Mahros, M.A., Abd-Elghany, S.M. and Sallam, K.I., 2021. Multi-drug-, methicillin-, and vancomycin-resistant Staphylococcus aureus isolated from ready-to-eat meat sandwiches: an ongoing food and public health concern. International Journal of Food Microbiology 346: 109165. 10.1016/j.ijfoodmicro.2021.109165
Meaden, S. and Koskella, B., 2013. Exploring the risks of phage application in the environment. Frontiers in Microbiology 4: 358. 10.3389/fmicb.2013.00358
Miedzybrodzki, R., Borysowski, J., Weber-Dabrowska, B., Fortuna, W., Letkiewicz, S., Szufnarowski, K., et al. 2012. Clinical aspects of phage therapy. Advances in Virus Research 83: 73–121. 10.1016/B978-0-12-394438-2.00003-7
Monteiro, R., Pires, D.P., Costa, A.R. and Azeredo, J., 2019. Phage therapy: going temperate? Trends in Microbiology 27: 368–378. 10.1016/j.tim.2018.10.008
Nikolic, P., Mudgil, P. and Whitehall, J., 2020. The in vitro antibacterial effect of permethrin and formaldehyde on Staphylococcus aureus. MicrobiologyOpen 9: e1054. 10.1002/mbo3.1054
Oduor, J., Kadija, E., Nyachieo, A., Mureithi, M.W. and Skurnik, M., 2020. Bioprospecting Staphylococcus phages with therapeutic and bio-control potential. Viruses (Basel) 12(2): 133. 10.3390/v12020133
Pang, Z., Raudonis, R., Glick, B.R., Lin, T.J. and Cheng, Z., 2019. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnology Advances 37: 177–192. 10.1016/j.biotechadv.2018.11.013
Ravindran, R. and Jaiswal, A.K., 2019. Wholesomeness and safety aspects of irradiated foods. Food Chemistry 285: 363–368. 10.1016/j.foodchem.2019.02.002
Samir, S., El-Far, A., Okasha, H., Mahdy, R., Samir, F. and Nasr, S., 2022. Isolation and characterization of lytic bacteriophages from sewage at an egyptian tertiary care hospital against methicillin-resistant Staphylococcus aureus clinical isolates. Saudi Journal of Biological Science 29: 3097–3106. 10.1016/j.sjbs.2022.03.019
Santos, S.B. and Azeredo, J., 2019. Bacteriophage-based biotechnological applications. Viruses (Basel) 11(8): 737. 10.3390/v11080737
Shimamori, Y., Pramono, A.K., Kitao, T., Suzuki, T., Aizawa, S.I., Kubori, T., et al. 2021. Isolation and characterization of a novel phage SaGU1 that infects Staphylococcus aureus clinical isolates from patients with atopic dermatitis. Current Microbiology 78: 1267–1276. 10.1007/s00284-021-02395-y
Su, Y.C., Hung, W.W., Lin, J.M., Chang, C.C., Chen, Y.H., Lai, Y.L., et al. 2020. Tracking the evolution of the two successful CC59 methicillin-resistant Staphylococcus aureus clones in Taiwan: the divergence time of the two clades is estimated to be the 1980s. International Journal of Antimicrobial Agents 56: 106047. 10.1016/j.ijantimicag.2020.106047
Takemura-Uchiyama, I., Uchiyama, J., Osanai, M., Morimoto, N., Asagiri, T., Ujihara, T., et al. 2014. Experimental phage therapy against lethal lung-derived septicemia caused by Staphylococcus aureus in mice. Microbes & Infections 16: 512–517. 10.1016/j.micinf.2014.02.011
Witte, S., Huijboom, L., Klamert, S., van de Straat, L., Hagens, S., Fieseler, L., et al. 2022. Application of bacteriophages EP75 and EP335 efficiently reduces viable cell counts of Escherichia coli O157 on beef and vegetables. Food Microbiology 104: 103978. 10.1016/j.fm.2022.103978
Wu, Y.N., Liu, X.M., Chen, Q., Liu, H., Dai, Y., Zhou, Y.J., et al. 2018. Surveillance for foodborne disease outbreaks in China, 2003 to 2008. Food Control 84: 382–388. 10.1016/j.foodcont.2017.08.010
Yang, M., Liang, Y., Huang, S., Zhang, J., Wang, J., Chen, H., et al. 2020. Isolation and characterization of the novel phages vB_VpS_BA3 and vB_VpS_CA8 for lysing vibrio parahaemolyticus. Frontiers in Microbiology 11: 259. 10.3389/fmicb.2020.00259
Zhang, L., Shahin, K., Soleimani-Delfan, A., Ding, H., Wang, H., Sun, L., et al. 2022b. Phage JS02, a putative temperate phage, a novel biofilm-degrading agent for Staphylococcus aureus. Letters in Applied Microbiology 75: 643–654. 10.1111/lam.13663
Zhang, F., Wu, S., Lei, T., Wu, Q., Zhang, J., Huang, J., et al. 2022a. Presence and characterization of methicillin-resistant Staphylococcus aureus co-carrying the multidrug resistance genes cfr and lsa (E) in retail food in China. International Journal of Food Microbiology 363: 109512. 10.1016/j.ijfoodmicro.2021.109512
Zhou, Y., Li, L., Han, K., Wang, L., Cao, Y., Ma, D., et al. 2022. A polyvalent broad-spectrum Escherichia phage Tequatro virus EP01 capable of controlling Salmonella and Escherichia coli contamination in foods. Viruses (Basel) 14. 10.3390/v14020286
Zhou, W.Y., Li, X., Osmundson, T., Shi, L., Ren, J. and Yan, H., 2018a. WGS analysis of ST9-MRSA-XII isolates from live pigs in China provides insights into transmission among porcine, human and bovine hosts. Journal of Antimicrobial Chemotherapy 73: 2652–2661. 10.1093/jac/dky245
Zhou, W.Y., Li, X., Shi, L., Wang, H.H. and Yan, H., 2018b. Novel SCCmec type XII methicillin-resistant Staphylococcus aureus isolates identified from a swine production and processing chain. Veterinary Microbiology 225: 105–113. 10.1016/j.vetmic.2018.09.007
Zhou, W.Y., Sun, S.F., Zhang, Y.S., Hu, Q., Zheng, X.F., Yang, Z.Q., et al. 2021. Isolation and characterization of a virulent bacteriophage for controlling Salmonella Enteritidis growth in ready-to-eat nixed-ingredient salads. Journal of Food Protection 84: 1629–1639. 10.4315/JFP-20-460
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