Creation of Pyocin Composition Against Laboratory and Clinical Pseudomonas aeruginosa Strains
DOI:
https://doi.org/10.15407/Keywords:
pyocins, composition creation, Pseudomonas aeruginosa, antibiotic resistance, clinical multidrug-resistant isolates, laboratory strainsAbstract
Pseudomonas aeruginosa belongs to the group of ESKAPE pathogens, which most often cause nosocomial infections and are characterized by a high level of antibiotic resistance. Bacteriocins are considered to be one of the promising substances that can be used as an additional means of influencing P. aeruginosa strains with multiple antibiotic resistance. The aim of this work was to evaluate the possibility of creating an effective composition from the minimum quantity of pyocins capable of inhibiting the growth of laboratory and clinical P. aeruginosa strains. Methods. The object of the study was P. aeruginosa bacteriocins (pyocins) isolated from 10 highly active producers. Analysis of pyocin’s activity and subsequent selection of the composition were carried out after assessing its influence on 51 cultures, which included laboratory strains, isolated from plant cultures, and clinical P. aeruginosa strains. Results. It was established that according to activity spectrum of the studied bacteriocins, pyocins 335, 333, 330, 13, and 332 can be referred to the most promising. To inhibit the growth of laboratory P. aeruginosa strains, it is sufficient to use pyocins 335 and 333 added with a third pyocin into the composition – 13 or 332. As for cultures isolated from plants, only pyocins 330 and 332 were characterized by high activity. In contrast, most pyocins influenced clinical isolates, which were multidrug-resistant to widely used antibiotics. The average activity of the selected pyocin composition 332+333+335 against laboratory cultures was 204.8×103 AU/mL and against clinical strains – 153.6×103 AU/mL. Conclusions. Thus, for the first time, the possibility of creating an effective composition of three pyocins that is capable of affecting both laboratory and clinical P. aeruginosa strains has been shown. The most optimal combination includes pyocins 332, 333, and 335, which contain S1, S2, S4, S5, and S9 bacteriocin subtypes. These substances do not exhibit mutual antagonism, bind to different receptors, and, due to DNase, tRNase, and pore-forming activities, inhibit the growth of all 51 cultures studied, represented by laboratory and isolated from plant strains, as well as clinical multidrug-resistant P. aeruginosa isolates.
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References
Ahmed, M., & Abdul Muhsin, Z. (2024). Synergistic Effect of Gentamicin and Iron Oxide Nanoparticles on phzM Gene of Pseudomonas aeruginosa. Mikrobiolohichnyi Zhurnal, 86(3), 27-39. https://doi.org/10.15407/microbiolj86.03.027
Ahmed, M., Al-Awadi, A., & Abbas, A. (2023). Focus on Synergistic Bacteriocin-Nanoparticles Enhancing Antimicrobial Activity Assay. Mikrobiolohichnyi Zhurnal, 85(6), 95-104. https://doi.org/10.15407/microbiolj85.06.095
Akereuke, U., Onwuezobe, I., Ekuma, A., Edem, E., Uko, N., Okon, R., Bawonda, E., & Ekpenyong, E. (2023). Molecular Profile of Metallo-β-Lactamase Producing Bacterial Isolates from Clinical Samples; South-South Nigeria Perspective. Mikrobiolohichnyi Zhurnal, 85(6), 15-25. https://doi.org/10.15407/microbiolj85.06.015
Alfarras, A., & Al-Daraghi, W. (2024). Characterization of Integron Genes of Clinical Isolates of Pseudomonas aeruginosa which Perform Resistance to Antibiotics and Biofilm Formation by these Strains. Mikrobiolohichnyi Zhurnal, 86(1), 3-13. https://doi.org/10.15407/microbiolj86.01.003
Amann, S., Neef, K., & Kohl, S. (2019). Antimicrobial resistance (AMR). European journal of hospital pharmacy: science and practice, 26(3), 175-177. https://doi.org/10.1136/ejhpharm-2018-001820
Arbune, M., Gurau, G., Niculet, E., Iancu, A. V., Lupasteanu, G., Fotea, S., Vasile, M. C., & Tatu, A. L. (2021). Prevalence of Antibiotic Resistance of ESKAPE Pathogens Over Five Years in an Infectious Diseases Hospital from South-East of Romania. Infection and drug resistance, 14, 2369-2378. https://doi.org/10.2147/IDR.S312231
Atanaskovic, I., Mosbahi, K., Sharp, C., Housden, N. G., Kaminska, R., Walker, D., & Kleanthous, C. (2020). Targeted Killing of Pseudomonas aeruginosa by Pyocin G Occurs via the Hemin Transporter Hur. Journal of molecular biology, 432(13), 3869-3880. https://doi.org/10.1016/j.jmb.2020.04.020
Balko, O. B., Zelena, L. B., Balko, O. I., Bobyr, N. A., Voitsekhovsky, V. G., & Avdeeva, L. V. (2024). Phenotypic and Genotypic Criteria for the Screening of Highly Active S-Type Pyocins Pseudomonas aeruginosa Producers. Mikrobiolohichnyi Zhurnal, 86(1), 39-50. https://doi.org/10.15407/microbiolj86.01.039
Balko, O. B. (2021). Interaction between S-Type Pyocins and Microcin-II-Like Bacteriocins in Pseudomonas aeruginosa. Mikrobiolohichnyi Zhurnal, 83(3), 72-80. https://doi.org/10.15407/microbiolj83.03.072
Balko, O. I., Balko, O. B. & Avdeeva, L. V. (2020). Bacteriocins of Some Groups of Gram-Negative Bacteria. Mikrobiolohichnyi Zhurnal, 82(3), 71-84. https://doi.org/10.15407/microbiolj82.03.071
Balko, O. B. (2019). Low Molecular Weight Pseudomonas aeruginosa Bacteriocins. Mikrobiolohichnyi Zhurnal, 81(6), 97-109. https://doi.org/10.15407/microbiolj81.06.097
Balko, O. I., Balko, O. B., & Avdeeva, L. V. (2019). Thermoactivation of Pseudomonas aeruginosa Pyocins. Mikrobiolohichnyi Zhurnal, 81(5), 85-97. https://doi.org/10.15407/microbiolj81.05.085
Balko, O. I., Avdeeva, L. V., Balko, O. B. (2018). Depositary Function of Pseudomonas aeruginosa Biofilm on Media with Different Carbon Source Concentration. Mikrobiolohichnyi Zhurnal, 80(6), 15-27. https://doi.org/10.15407/microbiolj80.06.015
Balko, O. I., Balko O. B., Yaroshenko L. V., Skorik M. A., & Avdeeva L. V. (2017). Resistance of Pseudomonas aeruginosa UCМ В-1 population to silver nanoparticles at early stages of biofilm formation. Mikrobiolohichnyi Zhurnal, 79(6), 71-81. https://doi.org/10.15407/microbiolj79.06.071
Balko, A. B., Balko, O. I., & Avdeeva, L. V. (2013a). [Biofilm formation by Pseudomonas aeruginosa strains of Ukrainian collection of microorganisms]. Mikrobiolohichnyi Zhurnal, 75(2), 50-56. [In russian].
Balko, A. B., Vidasov, V. V., & Avdeeva, L. V. (2013b). [Optimization of conditions of Pseudomonas aeruginosa bacteriocin induction]. Mikrobiolohichnyi Zhurnal, 75(1), 79-85. [In russian].
Balko, A. B. (2012). [Characteristic, properties, prospect of application of bacteriocins]. Mikrobiolohichnyi Zhurnal, 74(6), 99-106. [In russian].
Balko, A. B., & Avdeeva, L. V. (2012). [Screening of producers of bacteriocin-like substances active against Pseudomonas aeruginosa]. Mikrobiolohichnyi Zhurnal, 74(2), 8-13. [In russian].
Charkhian, H., Soleimannezhadbari, E., Bodaqlouei, A., Lotfollahi, L., Lotfi, H., Yousefi, N., Shojadel, E., & Gholinejad, Z. (2024). Assessment of bacteriocin production by clinical Pseudomonas aeruginosa isolates and their potential as therapeutic agents. Microbial cell factories, 23(1), 175. https://doi.org/10.1186/s12934-024-02450-w
Clinical and Laboratory Standards Institute (CLSI). (2024). Performance Standards for Antimicrobial Susceptibility Testing. 34th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute. https://clsi.org
Cubillo-Komarovova, P. J., Ledezma-Acevedo, R. E., Salazar-Cedeño, V., Murillo-Rodríguez, D., & Stern-Flores, D. (2024). Bacteriocins and its applications: mini-review. Tecnología en Marcha, 37(30), 79-89. https://doi.org/10.18845/tm.v37i9.7613
Denayer, S., Matthijs, S., & Cornelis, P. (2007). Pyocin S2 (Sa) kills Pseudomonas aeruginosa strains via the FpvA type I ferripyoverdine receptor. Journal of bacteriology, 189(21), 7663-7668. https://doi.org/10.1128/JB.00992-07
De Oliveira, D. M. P., Forde, B. M., Kidd, T. J., Harris, P. N. A., Schembri, M. A., Beatson, S. A., Paterson, D. L., & Walker, M. J. (2020). Antimicrobial Resistance in ESKAPE Pathogens. Clinical microbiology reviews, 33(3), e00181-19. https://doi.org/10.1128/CMR.00181-19
Elfadadny, A., Ragab, R. F., AlHarbi, M., Badshah, F., Ibáñez-Arancibia, E., Farag, A., Hendawy, A. O., De Los Ríos-Escalante, P. R., Aboubakr, M., Zakai, S. A., & Nageeb, W. M. (2024). Antimicrobial resistance of Pseudomonas aeruginosa: navigating clinical impacts, current resistance trends, and innovations in breaking therapies. Frontiers in microbiology, 15, 1374466. https://doi.org/10.3389/fmicb.2024.1374466
Elfarash, A., Dingemans, J., Ye, L., Hassan, A. A., Craggs, M., Reimmann, C., Thomas, M. S., & Cornelis, P. (2014). Pore-forming pyocin S5 utilizes the FptA ferripyochelin receptor to kill Pseudomonas aeruginosa. Microbiology (Reading, England), 160(Pt 2), 261-269. https://doi.org/10.1099/mic.0.070672-0
Elfarash, A., Wei, Q., & Cornelis, P. (2012). The soluble pyocins S2 and S4 from Pseudomonas aeruginosa bind to the same FpvAI receptor. Microbiologyopen, 1, 268-275. https://doi.org/10.1002/mbo3.27
EUCAST Disk Diffusion Method. (2024). Antimicrobial Susceptibility Testing. Version 12.0. The European Committee on Antimicrobial Susceptibility Testing. http://www.eucast.org
Fernández-Billón, M., Llambías-Cabot, A. E., Jordana-Lluch, E., Oliver, A., & Macià, M. D. (2023). Mechanisms of antibiotic resistance in Pseudomonas aeruginosa biofilms. Biofilm, 5, 100129. https://doi.org/10.1016/j.bioflm.2023.100129
FDA Susceptibility Test Interpretive Criteria (STIC). (2024). Breakpoint Implementation Toolkit. Food and Drug Administration.
Garmasheva I. L., Kovalenko N. K., Oleschenko L. T. (2018). Resistance to Antibiotics, Decarboxylase and Haemolytic Activities of Enterococci Isolated from Traditional Dairy Products. Mikrobiol Z, 80(1), 3-14. https://doi.org/10.15407/microbiolj80.01.003
Ghequire, M. G. K., & De Mot, R. (2014). Ribosomally encoded antibacterial proteins and peptides from Pseudomonas. FEMS Microbiol Rev, 38, 38523-38568. https://doi.org/10.1111/1574-6976.12079
Guliy, O. I., Bunin, V. D., Balko, A. B., Volkov, A. A., Staroverov, S., Karavaeva, O., & Ignatov, O. V. (2014). Effect of Sulfonamides on the Electrophysical Properties of Bacterial Cells. Anti-Infective Agents, 12(2), 191-197. https://doi.org/10.2174/2211352512666140630171501
Hooper, D. C., & Jacoby, G. A. (2016). Topoisomerase Inhibitors: Fluoroquinolone Mechanisms of Action and Resistance. Cold Spring Harbor perspectives in medicine, 6(9), a025320. https://doi.org/10.1101/cshperspect.a025320
Kotsofliak, O. I., Reva, O. M., & Tashyrev, O. B. (2004). [Taxonomic contribution and antagonistic properties of antarctic fluorescent bacteria of Pseudomonas genus]. Mikrobiolohichnyi Zhurnal, 66(2), 3-10. [In Ukrainian].
Kotsofliak, O. I., Reva, O. N., Kiprianova, E. A., & Smirnov, V. V. (2003). [Identification of the Pseudomonas genus bacteria by computer analysis]. Mikrobiolohichnyi Zhurnal, 65(6), 3-12. [In russian].
Kovalchuk, V. P., Kondratiuk, V. M., Kovalenko, I. M., Burkot, V. M. (2019). Phenotypic and Genotypic Determinants of Antibiotic Resistance of Gram-Negative Bacteria - Etiological Factors of Infectious Complications of War Wounds. Mikrobiol Z, 81(1), 61-71. https://doi.org/10.15407/microbiolj81.01.061
Langendonk, R. F., Neill, D. R., & Fothergill, J. L. (2021). The Building Blocks of Antimicrobial Resistance in Pseudomonas aeruginosa: Implications for Current Resistance-Breaking Therapies. Frontiers in cellular and infection microbiology, 11, 665759. https://doi.org/10.3389/fcimb.2021.665759
Lopetuso, L. R., Giorgio, M. E., Saviano, A., Scaldaferri, F., Gasbarrini, A., & Cammarota, G. (2019). Bacteriocins and Bacteriophages: Therapeutic Weapons for Gastrointestinal Diseases? International journal of molecular sciences, 20(1), 183. https://doi.org/10.3390/ijms20010183
Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B., Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T., & Monnet, D. L. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical microbiology and infection: the official publication of the European Society of Clinical Microbiology and Infectious Diseases, 18(3), 268-281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Ohkawa, I., Kageyama, M., & Egami, F. (1973). Purification and properties of pyocin S2. J Biochem, 73, 281-289.
Okshevsky, M., Regina, V. R., & Meyer, R. L. (2015). Extracellular DNA as a target for biofilm control. Current opinion in biotechnology, 33, 73-80. https://doi.org/10.1016/j.copbio.2014.12.002
Parret, A., & De Mot, R. (2000). Novel bacteriocins with predicted tRNase and pore-forming activities in Pseudomonas aeruginosa PAO1. Molecular microbiology, 35(2), 472-473. https://doi.org/10.1046/j.1365-2958.2000.01716.x
Pidgorskyi, V. S., Kotsofliak, O. I., Kiprianova, O. A., & Gvosdiak, O. R. (2007). Ukrainian collection of microorganisms. Catalogue of cultures. Kyiv: Naukova Dumka.
Ramirez, M. S., & Tolmasky, M. E. (2010). Aminoglycoside modifying enzymes. Drug resistance updates: reviews and commentaries in antimicrobial and anticancer chemotherapy, 13(6), 151-171. https://doi.org/10.1016/j.drup.2010.08.003
Roulová, N., Mot'ková, P., Brožková, I., & Pejchalová, M. (2022). Antibiotic resistance of Pseudomonas aeruginosa isolated from hospital wastewater in the Czech Republic. Journal of water and health, 20(4), 692-701. https://doi.org/10.2166/wh.2022.101
Sastre-Femenia, M. À., Fernández-Muñoz, A., Gomis-Font, M. A., Taltavull, B., López-Causapé, C., Arca-Suárez, J., Martínez-Martínez, L., Cantón, R., Larrosa, N., Oteo-Iglesias, J., Zamorano, L., Oliver, A., & GEMARA-SEIMC/CIBERINFEC Pseudomonas study Group (2023). Pseudomonas aeruginosa antibiotic susceptibility profiles, genomic epidemiology and resistance mechanisms: a nation-wide five-year time lapse analysis. The Lancet regional health. Europe, 34, 100736. https://doi.org/10.1016/j.lanepe.2023.100736
Soltani, S., Hammami, R., Cotter, P. D., Rebuffat, S., Said, L. B., Gaudreau, H., Bédard, F., Biron, E., Drider, D., & Fliss, I. (2021). Bacteriocins as a new generation of antimicrobials: toxicity aspects and regulations. FEMS microbiology reviews, 45(1), fuaa039. https://doi.org/10.1093/femsre/fuaa039
The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 14.0, 2024. http://www.eucast.org
Tooke, C. L., Hinchliffe, P., Bragginton, E. C., Colenso, C. K., Hirvonen, V. H. A., Takebayashi, Y., & Spencer, J. (2019). β-Lactamases and β-Lactamase Inhibitors in the 21st Century. Journal of molecular biology, 431(18), 3472-3500. https://doi.org/10.1016/j.jmb.2019.04.002
Versluis, D., Nijsse, B., Naim, M. A., Koehorst, J. J., Wiese, J., Imhoff, J. F., Schaap, P. J., van Passel, M. W. J., Smidt, H., & Sipkema, D. (2018). Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio. Genome biology and evolution, 10(1), 125-142. https://doi.org/10.1093/gbe/evx271
Zhao, H., Song, C. Y., Yin, R., Yi, Y. J., Yun, S. T., Li, Y. X., & Zhou, Y. X. (2021). Echinicola salinicaeni sp. nov., a novel bacterium isolated from saltern mud. Antonie van Leeuwenhoek, 114(11), 1915-1924. https://doi.org/10.1007/s10482-021-01650-3
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