Antifungal, Anti-Biofilm, and Anti-Phospholipase Effects of Pseudomonas aeruginosa Bacteriocins on Clinical Yeast Pathogens

Authors

  • ALI NABEEL AL-MIZEL Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq
  • HAMZIA ALI AJAH Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq https://orcid.org/0000-0002-0931-5995
  • RAGHAD ABDULLATIF ABUDLRAZAQ Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq https://orcid.org/0000-0003-4012-3673

Keywords:

Bacteriocin, Biofilm, Phospholipase, Candida, Cryptococcus

Abstract

Yeast infections pose a significant challenge around the world, especially with the rising of antifungal drug resistance. This study investigates the antifungal, anti-biofilm and anti-phospholipase activity of bacteriocins produced by the bacterium Pseudomonas aeruginosa against 12 yeast isolates which were selected from 57 according to their high resistance to commonly used antifungal drugs, high biofilm production and phospholipase production. Additionally, this study tested the viability of the yeast cells tested after exposure to the bacteriocin. Forty P. aeruginosa isolates were tested and the most potent bacteriocin producing isolate was selected. The partially purified pyocins had high antifungal activity with a range of 40.57 µg ml-1 to 81.15 µg ml-1 minimum inhibitory concentration (MIC) against multiple clinical and drug resistant Candida and Cryptococcus isolates and surpassed the conventionally used antifungal drugs. It also possessed strong anti-biofilm activity, though its anti-phospholipase activity is varied and isolate dependent, and the viability of the yeast cells was significantly reduced. The high antimicrobial activity of the bacteriocin shows its potential as a therapeutic agent against yeast infections, especially those with high antifungal resistance and biofilm production. These findings can be beneficial to improve patients’ outcome as more novel antifungal therapeutic drugs are needed.

References

Abid, S.A., Aziz, S.N., Saeed, N.A.-H.A.H., Mizil, S.N., Al-Kadmy, I.M.S., Hussein, N.H., Al-Saryi, N., Ibrahim, S.A. & Hussein, J.D. (2023). Investigation of virulence factors in microbial organisms that associated with public health risk isolates from different environmental regions. Al-Mustansiriyah Journal of Science, 33: 5. DOI: 10.23851/mjs.v33i5.1303

Adeyemo, R. O., Famuyide, I. M., Dzoyem, J. P., & Lyndy Joy, M. (2022). Anti-biofilm, antibacterial, and anti-quorum sensing activities of selected South African plants traditionally used to treat diarrhoea. Evidence-Based Complementary and Alternative Medicine: eCAM, 2022, 1307801. DOI:10.1155/2022/1307801

Al-Baqer, T. M., Al-Gharrawi, S. A. R., & Saeed, N. A. A. (2021). Causative microorganisms and antibiotics susceptibilities in children with urinary tract infection. Al-Mustansiriyah Journal of Science, 32(1): 5–9. DOI:10.23851/mjs.v32i1.948

Ali Hameed Al-Dabbagh, A., Ali Ajah, H. & Abdul Sattar Salman, J. (2023). Detection of virulence factors from Candida spp. Isolated from oral and vaginal candidiasis in Iraqi patients. Archives of Razi Institute, 78(1): 465–474. DOI:10.22092/ARI.2022.359464.2420

Alqahtani, A., Kopel, J. & Hamood, A. (2022). The in vivo and in vitro assessment of pyocins in treating Pseudomonas aeruginosa infections. Antibiotics (Basel, Switzerland), 11(10): 1366. DOI:10.3390/antibiotics11101366

Arastehfar, A., Carvalho, A., Nguyen, M.H., Hedayati, M.T., Netea, M.G., Perlin, D.S. & Hoenigl, M. (2020). COVID-19-Associated Candidiasis (CAC): An underestimated complication in the absence of immunological predispositions? Journal of Fungi, 6: 211. DOI: 10.3390/jof6040211

Bahuguna, A., Khan, I., Bajpai, V.K. & Kang, S.C. (2017). MTT assay to evaluate the cytotoxic potential of a drug. Bangladesh Journal of Pharmacology, 12(2): 8. DOI:10.3329/bjp.v12i2.30892

Ball, A.L., Augenstein, E.D., Wienclaw, T.M., Richmond, B.C., Freestone, C.A., Lewis, J.M., Thompson, J.S., Pickett, B.E. & Berges, B.K. (2022). Characterization of Staphylococcus aureus biofilms via crystal violet binding and biochemical composition assays of isolates from hospitals, raw meat, and biofilm-associated gene mutants. Microbial Pathogenesis, 167: 105554. DOI: 10.1016/j.micpath.2022.105554

Behrens, H.M., Lowe, E.D., Gault, J., Housden, N.G., Kaminska, R., Weber, T.M., Thompson, C.M. A., Mislin, G.L.A., Schalk, I.J., Walker, D., Robinson, C.V. & Kleanthous, C. (2020). Pyocin S5 import into Pseudomonas aeruginosa reveals a generic mode of bacteriocin transport. mBio, 11(2): 10-1128. DOI: 10.1128/mBio.03230-19

Beute, J.E., Kim, A.Y., Park, J.J., Yang, A., Torres-Shafer, K., Mullins, D.W. & Sundstrom, P. (2022). The IL-20RB receptor and the IL-20 signaling pathway in regulating host defense in oral mucosal candidiasis. Frontiers in Cellular and Infection Microbiology, 12: 979701. DOI: 10.3389/fcimb.2022.979701

Ellepola, A.N.B., Joseph, B.K. & Khan, Z.U. (2014). The postantifungal effect and phospholipase production of oral Candida albicans from smokers, diabetics, asthmatics, denture wearers and healthy individuals following brief exposure to subtherapeutic concentrations of chlorhexidine gluconate. Mycoses, 57(9): 553–559. DOI:10.1111/myc.12194

Fule, S.R., Das, D. & Fule, R.P. (2015). Detection of phospholipase activity of Candida albicans and non albicans isolated from women of reproductive age with vulvovaginal candidiasis in rural area. Indian Journal of Medical Microbiology, 33(1): 92–95. DOI:10.4103/0255-0857.148392

Garcia-Vidal, C., Sanjuan, G., Moreno-García, E., Puerta-Alcalde, P., Garcia-Pouton, N., Chumbita, M., Fernandez-Pittol, M., Pitart, C., Inciarte, A., Bodro, M., Morata, L., Ambrosioni, J., Grafia, I., Meira, F., Macaya, I., Cardozo, C., Casals, C., Tellez, A., Castro, P., Marco, F., García, F., Mensa, J., Martínez, J.A., Soriano, A. & COVID-19 Researchers Group. (2021). Incidence of co-infections and superinfections in hospitalized patients with COVID-19: A retrospective cohort study. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases, 27: 83–88. DOI: 10.1016/j.cmi.2020.07.041

Gow, N.A.R., Johnson, C., Berman, J., Coste, A.T., Cuomo, C.A., Perlin, D.S., Bicanic, T., Harrison, T.S., Wiederhold, N., Bromley, M., Chiller, T. & Edgar, K. (2022). The importance of antimicrobial resistance in medical mycology. Nature Communications, 13: 5352. DOI: 10.1038/s41467-022-32249-5

Haghighipour, S., Pourahmad, M., Noorbakhsh, M. & Mohammadi, R. (2019). Candida urinary tract infection among ICU patients in Isfahan, Iran. Archives of Clinical Infectious Diseases, 14. DOI: 10.5812/archcid.86472

Hamady, A. & Marei, Y. (2021). Detection of als1 and hwp1 genes involved in biofilm formation in Candida albicans isolated from catheter-associated candiduria. Microbes and Infectious Diseases, 2(3): 558–566. DOI: 10.21608/mid.2021.76052.1153

Hayashida, M.Z., Seque, C.A., Pasin, V.P., Enokihara, M.M.S.E. & Porro, A.M. (2017). Disseminated cryptococcosis with skin lesions: Report of a case series. Anais Brasileiros de Dermatologia, 92: 69–72. DOI: 10.1590/abd1806-4841.20176343

Hussein, M., Yassin, A. & El-Gelany, F. (2019). Characterization, virulence factors, and antifungal susceptibility of vulvovaginal Candida isolated from women at Qena, Egypt. Egyptian Journal of Microbiology, 54: 13–24. DOI: 10.21608/ejm.2019.10543.1091

Kakar, A., Sastré-Velásquez, L.E., Hess, M., Galgóczy, L., Papp, C., Holzknecht, J., Romanelli, A., Váradi, G., Malanovic, N. & Marx, F. (2022). The membrane activity of the amphibian temporin B peptide analog TB_KKG6K sheds light on the mechanism that kills Candida albicans. mSphere, 7: e0029022. DOI: 10.1128/msphere.00290-22

Karajacob, A.S., Azizan, N.B., Al-Maleki, A.R.M., Goh, J.P.E., Loke, M.F., Khor, H.M., Ho, G.F., Ponnampalavanar, S. & Tay, S.T. (2023). Candida species and oral mycobiota of patients clinically diagnosed with oral thrush. PloS One, 18: e0284043. DOI: 10.1371/journal.pone.0284043

Kielkopf, C.L., Bauer, W. & Urbatsch, I.L. (2020). Bradford assay for determining protein concentration. Cold Spring Harbor Protocols, 2020: 102269. DOI: 10.1101/pdb.prot102269

Lima, T., Gunnarsson, S.B., Coelho, E., Evtuguin, D. V., Correia, A., Coimbra, M.A., Cedervall, T. & Vilanova, M. (2022). β-glucan-functionalized nanoparticles down-modulate the proinflammatory response of mononuclear phagocytes challenged with Candida albicans. Nanomaterials (Basel, Switzerland), 12: 2475. DOI: 10.3390/nano12142475

Ling, H., Saeidi, N., Rasouliha, B.H. & Chang, M.W. (2010). A predicted S-type pyocin shows a bactericidal activity against clinical Pseudomonas aeruginosa isolates through membrane damage. FEBS Letters, 584: 3354–3358. DOI: 10.1016/j.febslet.2010.06.021

El-Ganiny, M.A., Yossef, E.N. & Kamel, A.H. (2021). Prevalence and antifungal drug resistance of nosocomial Candida species isolated from two university hospitals in Egypt. Current Medical Mycology, 7(1): 31–37. DOI: 10.18502/cmm.7.1.6181

Mohamed, A.A., Elshawadfy, A.M., Amin, G. & Askora, A. (2021). Characterization of R-pyocin activity against Gram-positive pathogens for the first time with special focus on Staphylococcus aureus. Journal of Applied Microbiology, 131(6): 2780–2792. DOI:10.1111/jam.15134

Montoya, M.C., Magwene, P.M. & Perfect, J.R. (2021). Associations between Cryptococcus genotypes, phenotypes, and clinical parameters of human disease: A review. Journal of Fungi (Basel, Switzerland), 7(4): 260. DOI:10.3390/jof7040260

Morse, S.A., Vaughan, P., Johnson, D. & Iglewski, B. H. (1976). Inhibition of Neisseria gonorrhoeae by a bacteriocin from Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy, 10(2): 354–362. DOI: 10.1128/AAC.10.2.354

Oluyombo, O., Penfold, C.N. & Diggle, S.P. (2019). Competition in biofilms between cystic fibrosis isolates of Pseudomonas aeruginosa is shaped by R-pyocins. mBio, 10(1): e01828-18. DOI: 10.1128/mBio.01828-18

O'Neill, J. (2014). Antimicrobial resistance: Tackling a crisis for the health and wealth of nations (The Review on Antimicrobial Resistance). United Kingdom: The Review on Antimicrobial Resistance. Available at: https://amr-review.org/

Pal, M. (2018). Morbidity and mortality due to fungal infections. Journal of Applied Microbiology and Biochemistry, 1(1): 1-3. DOI: 10.21767/2576-1412.100002.

Paškevičius, Š., Dapkutė, V., Misiūnas, A., Balzaris, M., Thommes, P., Sattar, A., Gleba, Y. & Ražanskienė, A. (2022). Chimeric bacteriocin S5-PmnH engineered by domain swapping efficiently controls Pseudomonas aeruginosa infection in murine keratitis and lung models. Scientific Reports, 12: 5865. DOI: 10.1038/s41598-022-09865-8

Perinelli, D., Campana, R., Skouras, A., Bonacucina, G., Cespi, M., Mastrotto, F., Baffone, W. & Casettari, L. (2018). Chitosan loaded into a hydrogel delivery system as a strategy to treat vaginal co-infection. Pharmaceutics, 10(1): 23. DOI: 10.3390/pharmaceutics10010023.

Sarker, S.D., Nahar, L. & Kumarasamy, Y. (2007). Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods, 42(4): 321-324. DOI: 10.1016/j.ymeth.2007.01.006

Taher, N.A. (2017). Antimicrobial effect of bacteriocin produced by Pediococcus pentosaceus on some clinical isolates. Al-Mustansiriyah Journal of Science, 27: 26–30. DOI: 10.23851/mjs.v27i5.163

Van de Veerdonk, F.L., Joosten, L.A.B. & Netea, M.G. (2015). The interplay between inflammasome activation and antifungal host defense. Immunological Reviews, 265: 172–180. DOI: 10.1111/imr.12280

Vechi, H.T., Theodoro, R.C., de Oliveira, A.L., da Silva Gomes, R.M., de Almeida Soares, R.D., Freire, M.G. & Baumgardt Bay, M. (2019). Invasive fungal infection by Cryptococcus neoformans var. grubii with bone marrow and meningeal involvement in a HIV-infected patient: A case report. BMC Infectious Diseases, 19: 220. DOI: 10.1186/s12879-019-3831-8

Vitális, E., Nagy, F., Tóth, Z., Forgács, L., Bozó, A., Kardos, G., Majoros, L. & Kovács, R. (2020). Candida biofilm production is associated with higher mortality in patients with candidaemia. Mycoses, 63(4): 352-360. DOI: 10.1111/myc.13049

Wang, J., Zhang, Z., Zhang, M., Yang, B., Wang, T., Sun, X., Chen, X., Zhang, M.Y., Guo, Z.Y. & Jiang, X. (2019). A rare primary Candida parapsilosis infection of the knee joint in a patient without predisposing factors: A case report. Medicine, 98(6): e14327. DOI: 10.1097/MD.0000000000014327

Zhu, B., Li, Z., Yin, H., Hu, J., Xue, Y., Zhang, G., Zheng, X., Chen, W., & Hu, X. (2022). Synergistic antibiofilm effects of pseudolaric acid A combined with fluconazole against Candida albicans via inhibition of adhesion and yeast-to-hypha transition. Microbiology Spectrum, 10(2): e01478-21. DOI: 10.1128/spectrum.01478-21.

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Published

2025-06-26

How to Cite

AL-MIZEL, A. N. ., AJAH, H. A. ., & ABUDLRAZAQ, R. A. . (2025). Antifungal, Anti-Biofilm, and Anti-Phospholipase Effects of Pseudomonas aeruginosa Bacteriocins on Clinical Yeast Pathogens. Borneo Journal of Resource Science and Technology, 15(1), 55–69. Retrieved from https://publisher.unimas.my/ojs/index.php/BJRST/article/view/7828