Abstract
The growing interest in bacteriophages and antibiotics’ combined use poses new challenges regarding this phenomenon’s accurate description. This study aimed to apply the PhageScore methodology to assess the phage-antibiotic combination activity in liquid bacterial culture. For this purpose, previously described Acinetobacter infecting phages vB_AbaP_AGC01, Aba-1, and Aba-4 and antibiotics (gentamicin, ciprofloxacin, meropenem, norfloxacin, and fosfomycin) were used to obtain a lysis curve of bacteriophages under antibiotic pressure. The experimental data were analyzed using the Fractional Inhibitory Concentration Index (FICI) and PhageScore methodology. The results obtained by this method clearly show differences between phage lytic activity after antibiotic addition. Thus, we present the potential use of the PhageScore method as a tool for characterizing the phage antibiotic synergy in liquid culture. Further, the optimization of the PhageScore for this purpose can help compare antibiotics and their outcome on bacteriophage lytic activity.
This is a preview of subscription content, log in via an institution to check access.
References
Aslam S, Courtwright AM, Koval C et al (2019) Early clinical experience of bacteriophage therapy in 3 lung transplant recipients. Am J Transplant 19:2631–2639. https://doi.org/10.1111/ajt.15503
Augustyniak A, Grygorcewicz B, Nawrotek P (2018) Isolation of multidrug resistant coliforms and their bacteriophages from swine slurry. Turkish J Vet Anim Sci 42:319–325. https://doi.org/10.3906/vet-1710-102
Bruttin A, Brüssow H (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49:2874–2878. https://doi.org/10.1128/AAC.49.7.2874-2878.2005
Chaudhry WN, Concepcion-Acevedo J, Park T et al (2017) Synergy and order effects of antibiotics and phages in killing Pseudomonas aeruginosa biofilms. PLoS ONE 12:e0168615. https://doi.org/10.1371/journal.pone.0168615
CLSI (2020) M100 Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement An informational supplement for global application developed through the Clinical and Laboratory Standards Institute consensus process
Colombet J, Robin A, Lavie L et al (2007) Virioplankton ‘pegylation’: use of PEG (polyethylene glycol) to concentrate and purify viruses in pelagic ecosystems. J Microbiol Methods 71:212–219. https://doi.org/10.1016/j.mimet.2007.08.012
Comeau AM, Tétart F, Trojet SN et al (2007) Phage-antibiotic synergy (PAS): β-lactam and quinolone antibiotics stimulate virulent phage growth. PLoS ONE 2:8–11. https://doi.org/10.1371/journal.pone.0000799
Galtier M, De Sordi L, Sivignon A et al (2017) Bacteriophages targeting adherent invasive Escherichia coli strains as a promising new treatment for Crohn’s disease. J Crohn’s Colitis 11:jjw224. https://doi.org/10.1093/ecco-jcc/jjw224
Grygorcewicz B, Grudziński M, Wasak A et al (2017) Bacteriophage-mediated reduction of Salmonella enteritidis in swine slurry. Appl Soil Ecol 119:179–182. https://doi.org/10.1016/j.apsoil.2017.06.020
Grygorcewicz B, Roszak M, Golec P et al (2020) Antibiotics Act with vB_AbaP_AGC01 phage against Acinetobacter baumannii in human heat-inactivated plasma blood and Galleria mellonella models. Int J Mol Sci 21:4390. https://doi.org/10.3390/ijms21124390
Grygorcewicz B, Wojciuk B, Roszak M et al (2021) Environmental phage-based cocktail and antibiotic combination effects on Acinetobacter baumannii biofilm in a human urine model. Microb Drug Resist 27:25–35. https://doi.org/10.1089/mdr.2020.0083
Jeon J, Park JH, Yong D (2019) Efficacy of bacteriophage treatment against carbapenem-resistant Acinetobacter baumannii in Galleria mellonella larvae and a mouse model of acute pneumonia. BMC Microbiol 19:70. https://doi.org/10.1186/s12866-019-1443-5
Jo A, Ding T, Ahn J (2016) Synergistic antimicrobial activity of bacteriophages and antibiotics against Staphylococcus aureus. Food Sci Biotechnol 25:935–940. https://doi.org/10.1007/s10068-016-0153-0
Kamal F, Dennis JJ (2015) Burkholderia cepacia complex phage-antibiotic synergy (PAS): antibiotics stimulate lytic phage activity. Appl Environ Microbiol 81:1132–1138. https://doi.org/10.1128/AEM.02850-14
Konopacki M, Grygorcewicz B, Dołęgowska B et al (2020) PhageScore: a simple method for comparative evaluation of bacteriophages lytic activity. Biochem Eng J. https://doi.org/10.1016/j.bej.2020.107652
Kvachadze L, Balarjishvili N, Meskhi T et al (2011) Evaluation of lytic activity of staphylococcal bacteriophage Sb-1 against freshly isolated clinical pathogens. Microb Biotechnol 4:643–650. https://doi.org/10.1111/j.1751-7915.2011.00259.x
LaVergne S, Hamilton T, Biswas B et al (2018) Phage therapy for a multidrug-resistant Acinetobacter baumannii craniectomy site infection. Open Forum Infect Dis 5:ofy064. https://doi.org/10.1093/ofid/ofy064
Lechowska J, Kordas M, Konopacki M et al (2019) Hydrodynamic studies in magnetically assisted external-loop airlift reactor. Chem Eng J 362:298–309. https://doi.org/10.1016/j.cej.2019.01.037
Lin Y, Chang RYK, Britton WJ et al (2018) Synergy of nebulized phage PEV20 and ciprofloxacin combination against Pseudomonas aeruginosa. Int J Pharm 551:158–165. https://doi.org/10.1016/j.ijpharm.2018.09.024
Liu CG, Green SI, Min L et al (2020) Phage-antibiotic synergy is driven by a unique combination of antibacterial mechanism of action and stoichiometry. MBio 11:1–19. https://doi.org/10.1128/mBio.01462-20
Loc-Carrillo C, Abedon ST (2011) Pros and cons of phage therapy. Bacteriophage 1:111–114. https://doi.org/10.4161/bact.1.2.14590
Łoś JM, Golec P, Węgrzyn G et al (2008) Simple method for plating Escherichia coli bacteriophages forming very small plaques or no plaques under standard conditions. Appl Environ Microbiol 74:5113–5120. https://doi.org/10.1128/AEM.00306-08
Łubowska N, Grygorcewicz B, Kosznik-Kwaśnicka K et al (2019) Characterization of the three new kayviruses and their lytic activity against multidrug-resistant Staphylococcus aureus. Microorganisms 7:471. https://doi.org/10.3390/microorganisms7100471
Nouraldin AAM, Baddour MM, Harfoush RAH, Essa SAM (2015) Bacteriophage-antibiotic synergism to control planktonic and biofilm producing clinical isolates of Pseudomonas aeruginosa. Alexandria J Med 52:99–105. https://doi.org/10.1016/j.ajme.2015.05.002
Regeimbal JM, Jacobs AC, Corey BW et al (2016) Personalized therapeutic cocktail of wild environmental phages rescues mice from Acinetobacter baumannii wound infections. Antimicrob Agents Chemother 60:5806–5816. https://doi.org/10.1128/AAC.02877-15
Roszak M, Dołe B, Cecerska-Heryc´ Elżbieta et al (2022) Bacteriophage–ciprofloxacin combination effectiveness depends on Staphylococcus aureus–Candida albicans dual-species communities growth model. Microbial Drug Resist. https://doi.org/10.1089/MDR.2021.0324
Sarker SA, McCallin S, Barretto C et al (2012) Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology 434:222–232. https://doi.org/10.1016/j.virol.2012.09.002
Schooley RT, Biswas B, Gill JJ et al (2017) Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother 61:e00954-e1017. https://doi.org/10.1128/AAC.00954-17
Szymczak M, Grygorcewicz B, Karczewska-Golec J et al (2020) Characterization of a unique Bordetella bronchiseptica vB_BbrP_BB8 bacteriophage and its application as an antibacterial agent. Int J Mol Sci 21:1403. https://doi.org/10.3390/ijms21041403
Tagliaferri TL, Jansen M, Horz H-PP (2019) Fighting pathogenic bacteria on two fronts: phages and antibiotics as combined strategy. Front Cell Infect Microbiol 9:22. https://doi.org/10.3389/fcimb.2019.00022
Townsend EM, Kelly L, Gannon L, Muscatt G, Dunstan R, Michniewski S, Sapkota H, Kiljunen SJ, Kolsi A, Skurnik M, Lithgow T, Millard AD, Jameson E (2020) Isolation and chacterisation of Klebsiella phages for phage therapy. PHAGE 2(1):26–42. https://doi.org/10.1089/phage.2020.0046
Zhang G, Zhao Y, Paramasivan S et al (2018) Bacteriophage effectively kills multidrug resistant Staphylococcus aureus clinical isolates from chronic rhinosinusitis patients. Int Forum Allergy Rhinol 8:406–414. https://doi.org/10.1002/alr.22046
Funding
This research was funded by the National Science Centre (Poland) within the project grant no. 2018/29/N/ST8/01043 (granted to B.G.). The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Grygorcewicz, B., Roszak, M., Rakoczy, R. et al. PhageScore-based analysis of Acinetobacter baumannii infecting phages antibiotic interaction in liquid medium. Arch Microbiol 204, 421 (2022). https://doi.org/10.1007/s00203-022-03020-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03020-7