Pseudomonas aeruginosa SWUC02 Cell-Free Culture as a Potential Antimicrobial Agent Against Household Antibiotics-Resistant Staphylococcus aureus

Authors

  • Kotchanat Srisangchun Department of Microbiology, Faculty of Science, Srinakharinwirot University, Bangkok, 10110, Thailand
  • Angkana Yoopom Department of Microbiology, Faculty of Science, Srinakharinwirot University, Bangkok, 10110, Thailand
  • Rasiyakapat Boonyangchanichkul Department of Microbiology, Faculty of Science, Srinakharinwirot University, Bangkok, 10110, Thailand
  • Prawat Aungpraphapornchai Department of Microbiology, Faculty of Science, Srinakharinwirot University, Bangkok, 10110, Thailand
  • Kwannan Nantavisai Department of Microbiology, Faculty of Medicine, Srinakharinwirot University, Bangkok, 10110, Thailand
  • Onanong Pringsulaka Department of Microbiology, Faculty of Science, Srinakharinwirot University, Bangkok, 10110, Thailand
  • Siriruk Sarawaneeyaruk Department of Microbiology, Faculty of Science, Srinakharinwirot University, Bangkok, 10110, Thailand

DOI:

https://doi.org/10.59796/jcst.V13N3.2023.1349

Keywords:

MRSA, S. aureus, antagonists, phenazine, Pseudomonas

Abstract

Contamination of household environments with pathogenic bacteria poses a significant risk of foodborne illnesses. This study aimed to investigate the effectiveness of cell-free culture obtained from Pseudomonas aeruginosa SWUC02 (CF-SWUC02) against Staphylococcus aureus, a common pathogen associated with food poisoning outbreaks. The antagonistic activity of P. aeruginosa SWUC02 and CF-SWUC02 against various pathogenic bacteria, particularly S. aureus, was assessed. The active antimicrobial compounds produced by P. aeruginosa SWUC02 demonstrated resistance to protease enzymes and high temperatures. Optimal culture conditions for inhibiting S. aureus were determined as LB media supplemented with 0.01% CuCl2, inoculated with 1x105 CFU.mL-1 of P. aeruginosa SWUC02, and incubated at 32°C with agitation (100 rpm) for 12 days. Eighty-six S. aureus isolates were collected from household environments and tested for antibiotic resistance, with 55 isolates exhibiting resistance to penicillin, and 17 isolates were  identified as methicillin-resistant S. aureus (MRSA). CF-SWUC02 demonstrated inhibitory effects against all S. aureus isolates, including MRSA. In conclusion, CF-SWUC02 displayed antagonistic activity against drug resistant S. aureus, suggesting its potential as a valuable resource for combating these pathogens. Furthermore, the presence of heat and protease stable antimicrobial compounds in CF-SWUC02 highlights the need for further investigation to explore their potential applications in the field of antimicrobial research.

References

Bharali, P., & Konwar, B. K. (2011). Production and physico-chemical characterization of a biosurfactant produced by Pseudomonas aeruginosa OBP1 isolated from petroleum sludge. Applied Biochemistry and Biotechnology, 164, 1444–1460. https://doi.org/10.1007/s12010-011-9225-z

Cardozo, V. F., Oliveira, A. G., Nishio, E. K., Perugini, M. R., Andrade, C. G., Silveira, W. D., ... & Nakazato, G. (2013). Antibacterial activity of extracellular compounds produced by a Pseudomonas strain against methicillin-resistant Staphylococcus aureus (MRSA) strains. Annals of Clinical Microbiology and Antimicrobials, 12(1), 1-8. https://doi.org/10.1186/1476-0711-12-12

Castric, P. A. (1975). Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Canadian Journal of Microbiology, 21(5), 613–618. https://doi.org/10.1139/m75-088

Clinical and Laboratory Standards Institute (CLSI). (2021). M100 Performance standards for antimicrobial susceptibility testing (31st ed.). Wayne, US: Clinical and Laboratory Standards Institute.

de Oliveira, A. G., Spago, F. R., Simionato, A. S., Navarro, M. O., da Silva, C. S., Barazetti, A. R., ... & Andrade, G. (2016). Bioactive organocopper compound from Pseudomonas aeruginosa inhibits the growth of Xanthomonas citri subsp. citri. Frontiers in Microbiology, 7, 113. https://doi.org/10.3389/fmicb.2016.00113

de Souza, J. T., & Raaijmakers, J. M. (2003). Polymorphisms within the prnD and pltC genes from pyrrolnitrin and pyoluteorin-producing Pseudomonas and Burkholderia spp. FEMS microbiology ecology, 43(1), 21-34. https://doi.org/10.1111/j.1574-6941.2003.tb01042.x

El-Sheshtawy, H. S., & Doheim, M. M. (2014). Selection of Pseudomonas aeruginosa for biosurfactant production and studies of its antimicrobial activity. Egyptian Journal of Petroleum, 23(1), 1-6. https://doi.org/10.1016/j.ejpe.2014.02.001.

Feghali, P. A. R. E., & Nawas, T. (2018). Pyocyanin: A powerful inhibitor of bacterial growth and biofilm formation. Madridge Journal of Case Reports and Studies, 3(1), 101–107. https://doi.org/10.18689/mjcrs-1000125

Frank, D. N., Feazel, L. M., Bessesen, M. T., Price, C. S., Janoff, E. N., & Pace, N. R. (2010). The human nasal microbiota and Staphylococcus aureus carriage. PloS one, 5(5), Article e10598. https://doi.org/10.1371/journal.pone.0010598

Guo, Y., Song, G., Sun, M., Wang, J., & Wang, Y. (2020). Prevalence and therapies of antibiotic-resistance in Staphylococcus aureus. Frontiers in Cellular and Infection Microbiology, 10. https://doi.org/10.3389/fcimb.2020.00107

Gupta, A., & Khare, S. K. (2007). Enhanced production and characterization of a solvent stable protease from solvent tolerant Pseudomonas aeruginosa PseA. Enzyme and Microbial Technology, 42(1), 11-16. https://doi.org/10.1016/j.enzmictec.2007.07.019.

Gurung, R. R., Maharjan, P., & Chhetri, G. G. (2020). Antibiotic resistance pattern of Staphylococcus aureus with reference to MRSA isolates from pediatric patients. Future Science OA, 6(4). Article FSO464. https://doi.org/10.2144/fsoa-2019-0122

Huang, C. W., Lin, Y. S., Huang, W. C., Lai, C. C., Chien, H. J., Hu, N. J., & Chen, J. H. (2022). Inhibition of the clinical isolates of Acinetobacter baumannii by Pseudomonas aeruginosa: In vitro assessment of a case-based study. Journal of Microbiology, Immunology and Infection, 55(1), 60–68. https://doi.org/10.1016/j.jmii.2020.11.006

Kerbauy, G., CP Vivan, A., C Simões, G., S Simionato, A., Pelisson, M., C Vespero, E., ... & Andrade, G. (2016). Effect of a metalloantibiotic produced by Pseudomonas aeruginosa on Klebsiella pneumoniae carbapenemase (kpc)-producing K. pneumoniae. Current Pharmaceutical Biotechnology, 17(4), 389–397. https://doi.org/10.2174/138920101704160215171649

Kimmig, A., Hagel, S., Weis, S., Bahrs, C., Löffler, B., & Pletz, M. W. (2021). Management of Staphylococcus aureus bloodstream infections. Frontiers in Medicine, 7. https://doi.org/10.3389/fmed.2020.616524

Le, H. H., Dalsgaard, A., Andersen, P. S., Nguyen, H. M., Ta, Y. T., & Nguyen, T. T. (2021). Large-scale Staphylococcus aureus foodborne disease poisoning outbreak among primary school children. Microbiology Research, 12(1), 43–52. https://doi.org/10.3390/microbiolres12010005

Lopes, L. P., Oliveira Jr, A. G., Beranger, J. P., Góis, C. G., Vasconcellos, F., San Martin, J. A., ... & Andrade, G. (2012). Activity of extracellular compounds of Pseudomonas sp. against Xanthomonas axonopodis in vitro and bacterial leaf blight in Eucalyptus. Tropical Plant Pathology, 37(4), 233–238. https://doi.org/10.1590/s1982-56762012000400001

Mermel, L. A., Allon, M., Bouza, E., Craven, D. E., Flynn, P., O'Grady, N. P., ... & Warren, D. K. (2009). Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 update by the Infectious Diseases Society of America. Clinical Infectious Diseases, 49(1), 1–45. https://doi.org/10.1086/599376

Ministry of Public Health (Thailand). (2020). MOPH Notification No. 416 (B.E. 2563 (2020)). Royal Thai Government Gazette. Retrieved February 2, 2023, http://food.fda.moph.go.th/law/data/announ_moph/P416.PDF

Mouyna, I., Hartl, L., & Latgé, J-P. (2013). β-1,3-glucan modifying enzymes in Aspergillus fumigatus. Frontiers in Microbiology, 4, 81. https://doi.org/10.3389/fmicb.2013.00081

Navarro, M. O. P., Dilarri, G., Simionato, A. S., Grzegorczyk, K., Dealis, M. L., Cano, B. G., ... & Andrade, G. (2020). Determining the targets of fluopsin C action on gram-negative and gram-positive bacteria. Frontiers in Microbiology, 11, Article 1076. https://doi.org/10.3389/fmicb.2020.01076

Navarro, M. O. P., Simionato, A. S., Pérez, J. C. B., Barazetti, A. R., Emiliano, J., Niekawa, E. T. G., ... & Andrade, G. (2019). Fluopsin C for treating multidrug-resistant infections: In vitro activity against clinically important strains and in vivo efficacy against carbapenemase-producing Klebsiella pneumoniae. Frontiers in Microbiology, 10, Article 2431. https://doi.org/10.3389/fmicb.2019.02431

Pai, V., Rao, V. I., & Rao, S. P. (2010). Prevalence and antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus [MRSA] isolates at a tertiary care hospital in Mangalore, South India. Journal of Laboratory Physicians, 2(2), 82-84. https://doi.org/10.4103/0974-2727.72155.

Patil, U., & Chaudhari, A. (2009). Purification and characterization of solvent-tolerant, thermostable, alkaline metalloprotease from alkalophilic Pseudomonas aeruginosa MTCC 7926. Journal of Chemical Technology and Biotechnology, 84(9), 1255-1262. https://doi.org/10.1002/jctb.2169

Raaijmakers, J. M., & Mazzola, M. (2012). Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annual Review of Phytopathology, 50(1), 403–424. https://doi.org/10.1146/annurev-phyto-081211-172908

Raaijmakers, J. M., Weller, D. M., & Thomashow, L. S. (1997). Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Applied and Environmental Microbiology, 63(3), 881–887. https://doi.org/10.1128/aem.63.3.881-887.1997

Rieusset, L., Rey, M., Muller, D., Vacheron, J., Gerin, F., Dubost, A., ... & Prigent‐Combaret, C. (2020). Secondary metabolites from plant‐associated Pseudomonas are overproduced in biofilm. Microbial Biotechnology, 13(5), 1562–1580. https://doi.org/10.1111/1751-7915.13598

Sapkota, J., Sharma, M., Jha, B., & Bhatt, C. P. (2019). Prevalence of Staphylococcus aureus isolated from clinical samples in a tertiary care hospital: A descriptive cross-sectional study. Journal of Nepal Medical Association, 57(220), 398-402. https://doi.org/10.31729/jnma.4673

Schneemann, I., Wiese, J., Kunz, A. L., & Imhoff, J. F. (2011). Genetic approach for the fast discovery of phenazine producing bacteria. Marine Drugs, 9(5), 772–789. https://doi.org/10.3390/md9050772

Sharma, P., Vaiwala, R., Parthasarathi, S., Patil, N., Verma, A., Waskar, M., ... & Ayappa, K. G. (2022). Interactions of surfactants with the bacterial cell wall and inner membrane: Revealing the link between aggregation and antimicrobial activity. Langmuir, 38(50), 15714-15728. https://doi.org/10.1101/2021.05.26.445833

Srisangchun, K., Surachat, K., Nantavisai, K., Pringsulaka, O., & Sarawaneeyaruk, S. (2023, January 13–16). Genomic insights into antimicrobial-producing Pseudomonas aeruginosa SWUC02 [Conference presentation]. 12th International Conference on Bioscience, Biochemistry and Bioinformatics (ICBBB 2023), Tokyo, Japan. https://doi.org/10.1145/3586139.3586142 (in press)

Sudyoung, N., Tokuyama, S., Krajangsang, S., Pringsulaka, O., & Sarawaneeyaruk, S. (2020). Bacterial antagonists and their cell-free cultures efficiently suppress canker disease in citrus lime. Journal of Plant Diseases and Protection, 127(2), 173–181. https://doi.org/10.1007/s41348-019-00295-9

Tibebu, L., Belete, Y., Tigabu, E., & Tsegaye, W. (2021). Prevalence of Staphylococcus aureus, methicillin-resistant Staphylococcus aureus and potential risk factors in selected dairy farms at the interface of animal and human in Bishoftu, Ethiopia. Veterinary Medicine: Research and Reports, Volume 12, 241–251. https://doi.org/10.2147/vmrr.s331968

Tishyadhigama, P., Dejsirilert, S., Thongmali, O., Sawanpanyalert, P., Aswapokee, N., & Piboonbanakit, D. (2009). Antimicrobial resistance among clinical isolates of Staphylococcus aureus in Thailand from 2000 to 2005. Journal of the Medical Association of Thailand, 92(4), S8–S18.

Traub, W. H., & Leonhard, B. (1995). Heat stability of the antimicrobial activity of sixty-two antibacterial agents. Journal of Antimicrobial Chemotherapy, 35(1), 149-154. https://doi.org/10.1093/jac/35.1.149

Wonghirundecha, T., Monpangtiem, K., Butkarn, C., Duangkaew, J., Saengpakdi, M., Jankaew, S., … & Thammawijaya, P. (2019). An outbreak investigation of food poisoning in Buddhist ceremony, Mueang District, Yasothon Province, Thailand, 2018. Weekly Epidemiological Surveillance Report, 50(4), 49-58.

Yanti, N., Diraphat, P., & Siripanichgon, K. (2015, April 24). Study of community-onset and hospital-onset of methicillin-resistant Staphylococcus aureus infections at Taksin hospital, Bangkok [Conference presentation]. RSU National Research Conference, Pathum Thani, Thailand. https://doi.nrct.go.th/ListDoi/Download/110364/4dbfcaaa33869ce025a25cf02f58cd0a?Resolve_DOI=10.14458/RSU.res.2015.178

Zhang, L., Tian, X., Kuang, S., Liu, G., Zhang, C., & Sun, C. (2017). Antagonistic activity and mode of action of phenazine-1-carboxylic acid, produced by marine bacterium Pseudomonas aeruginosa pa31x, against vibrio anguillarum in vitro and in a zebrafish in vivo model. Frontiers in Microbiology, 8, Article 289. https://doi.org/10.3389/fmicb.2017.00289

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Published

2023-08-30

How to Cite

Srisangchun, K. ., Yoopom, A. ., Boonyangchanichkul, R. ., Aungpraphapornchai, P. ., Nantavisai, K. ., Pringsulaka, O., & Sarawaneeyaruk, S. . (2023). Pseudomonas aeruginosa SWUC02 Cell-Free Culture as a Potential Antimicrobial Agent Against Household Antibiotics-Resistant Staphylococcus aureus. Journal of Current Science and Technology, 13(3), 683–695. https://doi.org/10.59796/jcst.V13N3.2023.1349

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Research Article