Isolation and characterization of bacteriophage SA-19 and investigation of antibiofilm effect against clinical strains

Year 2024, Volume: 28 Issue: 2, 505 - 515, 28.06.2025

Damla Damar Çelik , Berna Özbek Çelik

Abstract

Because the emergence of antimicrobial resistance worldwide and alternative treatment strategies against Staphylococcus aureus infections are still being sought, we investigated a new bacteriophage with a lytic effect against S. aureus strains in this study. Then, we isolated potentially therapeutic lytic S. aureus phage from seawater and determined the biological characterization and in vitro lytic effect against various clinical bacterial strains. As a result, our study provides evidence of phage application for S. aureus strains, combination studies with conventional antibiotics as an alternative treatment option in clinical.

Keywords

Phage-antibiotic combination , Staphylococcus aureus , bacteriophage , biofilm

References

• [1] Wang J, Zhao F, Sun H, Wang Q, Zhang C, Liu W, Zou L, Pan Q, Ren H. Isolation and characterization of the Staphylococcus aureus bacteriophage vB_SauS_SA2. AIMS Microbiol. 2019; 5(3): 285. http://doi.org/10.3934/microbiol.2019.3.285.
• [2] Chessa D, Ganau G, Mazzarello V. An overview of Staphylococcus epidermidis and Staphylococcus aureus with focus on developing countries. J Infect Dev Ctries. 2015; 9(06): 547–550. http://doi.org/10.3855/jidc.6923.
• [3] Kazmierczak Z, Gorski A, Dabrowska K. Facing antibiotic resistance: Staphylococcus aureus phages as a medical tool. Viruses. 2014; 6(7): 2551–2570. http://dx.doi.org/10.3390/v6072551.
• [4] Ganaie MY, Qureshi S, Kashoo Z, Wani SA, Hussain MI, Kumar R, Maqbool R, Sikander P, Banday MS, Malla WA, Mondal P, Khan RIN. Isolation and characterization of two lytic bacteriophages against Staphylococcus aureus from India: newer therapeutic agents against bovine mastitis. Vet Res Commun. 2018; 42: 289–295. https://doi.org/10.1007/s11259-018-9736-y.
• [5] Golkar Z, Bagasra O, Pace DG. Bacteriophage therapy: A potential solution for the antibiotic resistance crisis. J Infect Dev Ctries. 2014; 8(2): 129-136. http://doi.org/10.3855/jidc.3573.
• [6] Chanishvili N. Literature review of the practical application of bacteriophage research. Nova Science Publishers, Incorporated, 2012.
• [7] Bruttin A, Brüssow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother. 2005; 49(7): 2874-2878. http://doi.org/10.1128/aac.49.7.2874-2878.2005.
• [8] Sylwia Bloch S, Dydecka A, Topka G, Necel A, Jakubowska-Deredas M, Narajczyk M, Richert M, Mieszkowska A, Wróbel B, Węgrzyn G, Węgrzyn A. Biodiversity of bacteriophages: Morphological and biological properties of a large group of phages isolated from urban sewage. Sci Rep. 2016; 6(1): 34338. http://doi.org/10.1038/srep34338.
• [9] Yuan Y, Gao M. Characteristics and complete genome analysis of a novel jumbo phage infecting pathogenic Bacillus pumilus causing ginger rhizome rot disease. Arch Virol. 2016; 161: 3597–3600. http://doi.org/10.1007/s00705-016-3053-y.
• [10] Fernandes S, Sao-Jose C. More than a hole: The holin lethal function may be required to fully sensitize bacteria to the lytic action of canonical endolysins. Mol Microbiol. 2016; 102(1): 92–106. http://doi.org/10.1111/mmi.13448.
• [11] Chang Y, Shin H, Lee Jh, Park CJ, Paik SY, Ryu S. Isolation and genome characterization of the virulent Staphylococcus aureus bacteriophage SA97. Viruses. 2015; 7(10): 5225–5242. http://doi.org/10.3390/v7102870.
• [12] Heaton CJ, Gerbig GR, Sensius LD, Patel V, Smith TC. Staphylococcus aureus epidemiology in wildlife: A systematic review. Antibiotics. 2020; 9(2): 89. http://doi.org/10.3390/antibiotics9020089.
• [13] Branston SD, Wright J, Keshavarz-Moore E. A nonchromatographic method for the removal of endotoxins from bacteriophages. Biotechnol Bioeng. 2015; 112(8): 1714–1719. https://doi.org/10.1002/bit.25571.
• [14] Samir S, El-Far A, Okasha H, Mahdy R, Samir F, Nasr S. Isolation and characterization of lytic bacteriophages from sewage at an Egyptian tertiary care hospital against methicillin-resistant Staphylococcus aureus clinical isolates. Saudi J Biol Sci. 2022; 29(5): 3097-3106. http://doi.org/10.1016/j.sjbs.2022.03.019.
• [15] Rai A, Khairnar K. Isolation and characterization of bacteriophage against wastewater isolates of methicillin-resistant Staphylococcus aureus. Jundishapur J Microbiol. 2021; 14(9). http://doi.org/10.5812/jjm.119291.
• [16] Kumari, S, Harjai K, Chhibber S. Evidence to support the therapeutic potential of bacteriophage Kpn5 in burn wound infection caused by Klebsiella pneumoniae in BALB/c mice. J Microbiol Biotechnol. 2010; 20: 935-941. http://doi.org/10.4014/jmb.0909.09010.
• [17] Fortier LC, Sekulovic O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence. 2013; 4(5): 354-365. https://doi.org/10.4161/viru.24498.
• [18] Wang D, Jiang Y, Xiao S, Wang M, Liu Q, Huang L, Xue C, Wang Q, Liu T, Shao H, McMinn A. Characterization and genome analysis of a novel alteromonas phage JH01 isolated from the Qingdao coast of China. Curr Microbiol. 2019; 76:1256–1263. http://doi.org/10.1007/s00284-019-01751-3.
• [19] Jiang Y, Xu Q, Jiang L, Zheng R. Isolation and Characterization of a lytic Staphylococcus aureus Phage WV against Staphylococcus aureus biofilm. Intervirology. 2021; 64(4): 169-177. http://doi.org/10.1159/000515282.
• [20] Hagens S, Loessner MJ. Bacteriophage for biocontrol of foodborne pathogens: Calculations and considerations. Curr. Pharm. Biotechnol. 2010;11(1): 58-68. http://doi.org/10.2174/138920110790725429.
• [21] Esmaeilzadeh MR, Sabzi S, Hajihossein Tabrizi A. Isolation and in vitro characterization of specific bacteriophages against Methicillin-Resistant Staphylococcus aureus. Inf Epidemiol Microbiol. 2022; 8(2):121-128. http://doi.org/10.52547/iem.8.2.121.
• [22] Toro H, Price SB, McKee S, Hoerr FJ, Krehling J, Perdue M, Bauermeister L. Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis. 2005; 49(1): 118. https://doi.org/10.1637/7286-100404R.
• [23] Gill JJ, Hyman P. Phage choice, isolation, and preparation for phage therapy. Curr Pharm Biotechnol. 2010; 11(1): 2-14. https://doi.org/10.2174/138920110790725311.
• [24] Akturk E, Oliveira H, Santos SB, Costa S, Kuyumcu S, Melo LD, Azeredo J. Synergistic action of phage and antibiotics: Parameters to enhance the killing efficacy against mono and dual-species biofilms. Antibiotics. 2019; 8(3): 103. http://doi.org/10.3390/antibiotics8030103.
• [25] Shimamori Y, Pramono AK, Kitao T, Suzuki T, Aizawa SI, Kubori T, Nagai H, Takeda S, Ando H. Isolation and characterization of a novel phage SaGU1 that infects Staphylococcus aureus clinical isolates from patients with atopic dermatitis. Curr Microbiol. 2021; 78: 1267-1276. http://doi.org/10.1007/s00284-021-02395-y.
• [26] Flemming HC, Wuertz S. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol. 2019; 17(4): 247-260. http://doi.org/10.1038/s41579-019-0158-9.
• [27] Shrestha LB, Foster C, Rawlinson W, Tedla N, Bull RA. Evolution of the SARS‐CoV‐2 omicron variants BA. 1 to BA. 5: Implications for immune escape and transmission. Rev Med Virol. 2022; 32(5): e2381. http://doi.org/10.1002/rmv.2381.
• [28] Kumaran D, Taha M, Yi Q, Ramirez-Arcos S, Diallo JS, Carli A, Abdelbary H. Does treatment order matter? Investigating the ability of bacteriophage to augment antibiotic activity against Staphylococcus aureus biofilms. Front Microbiol 2018; 9: 127. http://doi.org/10.3389/fmicb.2018.00127.
• [29] Dickey J, Perrot V. Adjunct phage treatment enhances the effectiveness of low antibiotic concentration against Staphylococcus aureus biofilms in vitro. PloS One. 2019; 14(1): e0209390. http://doi.org/10.1371/journal.pone.0209390.
• [30] Chaudhry WN, Concepcion-Acevedo J, Park T, Andleeb S, Bull JJ, Levin BR. Synergy and order effects of antibiotics and phages in killing Pseudomonas aeruginosa biofilms. PloS One. 2017; 12(1): e0168615. http://doi.org/10.1371/journal.pone.0168615.
• [31] Coulter LB, McLean RJ, Rohde RE, Aron GM. Effect of bacteriophage infection in combination with tobramycin on the emergence of resistance in Escherichia coli and Pseudomonas aeruginosa biofilms. Viruses. 2014; 6(10): 3778–86. http://doi.org/10.3390/v6103778.
• [32] Yuan Y, Wang L, Li X, Tan D, Cong C, Xu Y. Efficacy of a phage cocktail in controlling phage resistance development in multidrug resistant Acinetobacter baumannii. Virus Res. 2019; 272: 197734. https://doi.org/10.1016/j.virusres.2019.197734.
• [33] Fischer S, Kittler S, Klein G, Glünder G. Microplate-Test for the rapid determination of bacteriophage-susceptibility of Campylobacter İsolates—Development and validation. PLoS One. 2013; 8(1): e53899 http://doi.org/10.1371/journal.pone.0053899.
• [34] Karaynir A, Salih H, Bozdoğan B, Güçlü Ö, Keskin D. Isolation and characterization of Brochothrix phage ADU4. Virus Res. 2022; 321: 198902. https://doi.org/10.1016/j.virusres.2022.198902.
• [35] Yu YP, Gong T, Jost G, Liu WH, Ye DZ, Luo ZH. Isolation and characterization of five lytic bacteriophages infecting a Vibrio strain closely related to Vibrio owensii. FEMS Microbiol. Lett. 2013; 348(2): 112-119. http://doi.org/10.1111/1574-6968.12277.
• [36] Stepanovic S, Vukovic D, Dakic I, Savic B ve Svabic-Vlahovic M. A modified microtiter-plate test for quantification of Staphylococcal biofilm formation. J Microbiol Methods. 2000; 40(2): 175–179. http://doi.org/10.1016/S0167-7012(00)00122-6.
• [37] CLSI, Clinical & Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. M100. 2022. https://clsi.org/(accessed July 01, 2023).