Pyocyanin derived from the marine sponge-associated bacterium, Pseudomonas aeruginosa P1.S9, has the potential as antibacterial

##plugins.themes.bootstrap3.article.sidebar##

PDF
DOI https://doi.org/10.13057/biodiv/d251113
Issue
Vol. 25 No. 11 (2024)
Section
Articles
Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

##plugins.themes.bootstrap3.article.main##

DOVA KELVIN MESRIAN
Department of Biology, Faculty of Mathematics and Natural Sciences, Institut Pertanian Bogor. Jl. Agatis, IPB Dramaga Campus, Bogor 16680, West Java, Indonesia
RIKA INDRI ASTUTI
Department of Biology, Faculty of Mathematics and Natural Sciences, Institut Pertanian Bogor. Jl. Agatis, IPB Dramaga Campus, Bogor 16680, West Java, Indonesia
MUHAMMAD EKA PRASTYA
Research Center for Pharmaceutical Ingredients and Traditional Medicine, National Research and Innovation Agency (BRIN). PUSPIPTEK Complex, Setu, South Tangerang 15134, Banten, Indonesia
ARIS TRI WAHYUDI ♥
Department of Biology, Faculty of Mathematics and Natural Sciences, Institut Pertanian Bogor. Jl. Agatis, IPB Dramaga Campus, Bogor 16680, West Java, Indonesia

Abstract

Abstract. Mesrian DK, Astuti RI, Prastya ME, Wahyudi AT. 2024. Pyocyanin derived from the marine sponge-associated bacterium, Pseudomonas aeruginosa P1.S9, has the potential as antibacterial. Biodiversitas 25: 4139-4147. Sponge-associated bacteria are a prolific source of secondary metabolites. Among them, pyocyanin-producing Pseudomonas aeruginosa is a subject of great interest. Pyocyanin is a blue-green pigment known for its enormous biological activity, one of the most notable being antimicrobial. Therefore, this study was performed to optimize the production, to characterize the chemical structure, and to test the antimicrobial activity of pyocyanin. As the sole isolate used, Pseudomonas aeruginosa P1.S9 provided a fundamental premise for pyocyanin synthesis by revealing the presence of phzM and phzS genes. The proteins generated from these genes were highly compatible with two enzymes involved in the pyocyanin production pathway. During the optimization, the maximum level of pyocyanin produced was 29.057±0.691 µg mL-1. The concentration was obtained using a modified King's A medium incubated at 27°C within four days. To assess its purity, the chemical structure of pyocyanin was confirmed by several spectroscopic techniques including UV-Visible (UV-Vis), Fourier Transform Infrared (FT-IR), and Nuclear Magnetic Resonance (1HNMR). All test results closely resemble purified pyocyanin compared to several prior studies. In terms of antimicrobial activity, pyocyanin was effective against ATCC strains of Bacillus subtilis, Escherichia coli, Pseudomonas aeruginosa, and Staphylococcus aureus. Its strongest minimum inhibitory concentration (MIC) was 62.5 µg mL-1 against Bacillus subtilis. Subsequently, the accumulation of reactive oxygen species (ROS) as a major mechanism of pyocyanin antibacterial activity has also been verified. The bacterial pathogens cells treated with pyocyanin displayed a brighter luminescence compared to the control without pyocyanin after the addition of 2',7'-dichlorodihydrofluorescein diacetate (H2DCF-DA). Ultimately, the present work comprehensively characterized pyocyanin's promising producer and antibacterial properties.

##plugins.themes.bootstrap3.article.details##

References
Abdelaziz AA, Kamer AMA, Al-Monofy KB, Al-Madboly LA. 2022. A purified and lyophilized Pseudomonas aeruginosa derived pyocyanin induces promising apoptotic and necrotic activities against MCF-7 human breast adenocarcinoma. Microb Cell Fact 21 (1): 262. DOI: 10.1186/s12934-022-01988-x.
Abuohashish HM, El-Sharkawy AS. 2023. Biotechnological and pharmacological assessment of pyocyanin from marine Pseudomonas otitidis EGY-NIOF-A1 as an antimicrobial agent against clinical pathogens. Curr Res Biotechnol 6: 100156. DOI: 10.1016/j.crbiot.2023.100156.
Amjad S, Nisar S, Bhat AA, Frenneaux MP, Fakhro K, Haris M, Bagga P. 2021. Role of NAD+ in regulating cellular and metabolic signaling pathways. Mol Metab 49: 101195. DOI: 10.1016/j.molmet.2021.101195.
Bandara JMBMG, Arunakumara KKIU. 2020. Development of low-cost growing media for Spirulina using alternative carbon sources. Vidyodaya J Sci 23 (1): 41-47. DOI: 10.31357/vjs.v23i01.4679.
Bhargava N, Sharma P, Capalash N. 2014. Pyocyanin stimulates quorum sensing-mediated tolerance to oxidative stress and increases persister cell populations in Acinetobacter baumannii. Infect Immun 82 (8): 3417-3425. DOI: 10.1128/IAI.01600-14.
Botros HG, Legrand P, Pagan C, Bondet V, Weber P, Ben?Abdallah M, Bourgeron T. 2013. Crystal structure and functional mapping of human ASMT, the last enzyme of the melatonin synthesis pathway. J Pineal Res 54 (1): 46-57. DOI: 10.1111/j.1600-079x.2012.01020.x.
Brinkmann CM, Marker A, Kurtböke DI. 2017. An overview on marine sponge-symbiotic bacteria as unexhausted sources for natural product discovery. Diversity 9 (4): 40. DOI: 10.3390/d9040040.
Claudel M, Schwarte JV, Fromm KM. 2020. New antimicrobial strategies based on metal complexes. Chemistry 2 (4): 849-899. DOI: 10.3390/chemistry2040056.
CLSI [Clinical and Laboratory Standards Institute]. 2020. Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standars Institute, Pennsylvania.
Dahihande AS, Thakur NL. 2019. Temperature?and size?associated differences in the skeletal structures and osculum cross?sectional area influence the pumping rate of contractile sponge Cinachyrella cf. cavernosa. Mar Ecol 40 (5): e12565. DOI: 10.1111/maec.12565.
Dange SS, Gulve RM, Deshmukh RB, Phatake YB, Dange SR. 2019. Pyocyanin: Process optimization and evaluation of its antimicrobial activity. J Exp Biol Agric Sci 7: 494-504. DOI: 10.18006/2019.7(5).494.504.
Darwesh OM, Barakat KM, Mattar MZ, Sabae SZ, Hassan SH. 2019. Production of antimicrobial blue green pigment pyocyanin by marine Pseudomonas aeruginosa. Biointerface Res Appl Chem 9 (5): 4334-4339. DOI: 10.33263/BRIAC95.334339.
Diggle SP, Whiteley M. 2020. Microbe profile: Pseudomonas aeruginosa: Opportunistic pathogen and lab rat. Microbiology 166: 30-33. DOI: 10.1099/mic.0.000860.
Dong L, Pang J, Wang X, Zhang Y, Li G, Hu X, You X. 2020. Mechanism of pyocyanin abolishment caused by mvaT mvaU double knockout in Pseudomonas aeruginosa PAO1. Virulence 11 (1): 57-67. DOI: 10.1080/21505594.2019.1708052.
Duddy OP, Bassler BL. 2021. Quorum sensing across bacterial and viral domains. PLoS Pathog 17: e1009074. DOI: 10.1371/journal.ppat.1009074.
El-Fouly MZ, Sharaf AM, Shahin AAM, El-Bialy HA, Omara AMA. 2015. Biosynthesis of pyocyanin pigment by Pseudomonas aeruginosa. J Radiat Res Appl Sci 8: 36-48. DOI: 10.1016/j.jrras.2014.10.007.
Essar DW, Eberly L, Hadero A. 1990. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: Interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol 172 (2): 884-900.
Fazeli N, Momtaz H. 2014. Virulence gene profiles of multidrug-resistant Pseudomonas aeruginosa isolated from Iranian hospital infections. Iran Red Crescent Med J 16 (10): e15722. DOI: 10.5812/ircmj.15722.
Feghali P, Nawas T. 2018. Extraction and purification of pyocyanin: A simpler and more reliable method. MOJ Toxicol 4 (6): 417-422. DOI: 10.15406/MOJT.2018.04.00139.
Gahlout M, Chauhan PB, Prajapati H, Tandel N, Rana S, Solanki D, Patel N. 2021. Characterization, application and statistical optimization approach for enhanced production of pyocyanin pigment by Pseudomonas aeruginosa DN9. Syst Microbiol Biomanuf 1 (4): 459-470. DOI: 10.1007/s43393-021-00033-z.
Giordano D. 2020. Bioactive molecules from extreme environments. Mar drugs 18 (12): 640. DOI: 10.3390/md18120640.
Goncalves T, Vasconcelos U. 2021. Colour me blue: The history and the biotechnological potential of pyocyanin. Molecules 26 (4): 927. DOI: 10.3390/molecules26040927.
Hamad MN, Marrez DA, El-Sherbieny SM. 2020. Toxicity evaluation and antimicrobial activity of purified pyocyanin from Pseudomonas aeruginosa. Biointerface Res Appl Chem 10 (6): 6974-6990. DOI: 10.33263/BRIAC106.69746990.
Jabbar AT, Aziz RA, Al Marjani MF. 2020. Extraction, purification and characterization of pyocyanin pigment from Pseudomonas aeruginosa and testing its biological efficacy. Biochem Cell Arch 20 (2): 5585-5592.
Jablonska J, Augustyniak A, Dubrowska K, Rakoczy R. 2023. The two faces of pyocyanin-why and how to steer its production. World J Microbiol Biotechnol 39: 103. DOI: 10.1007/s11274-023-03548-w.
Khudhair ZY, Jameel ZJ, Ammari A. 2021. Molecular effect of pyocyanin on dermatological isolates of Candida albicans. Biochem Cell Arch 21 (1): 187-190.
Marey MA, Abozahra R, El-Nikhely NA, Kamal MF, Abdelhamid SM, El-Kholy MA. 2024. Transforming microbial pigment into therapeutic revelation: extraction and characterization of pyocyanin from Pseudomonas aeruginosa and its therapeutic potential as an antibacterial and anticancer agent. Microb Cell Fact 23 (1): 174. DOI: 10.1186/s12934-024-02438-6.
Meirelles LA, Newman DK. 2018. Both toxic and beneficial effects of pyocyanin contribute to the lifecycle of Pseudomonas aeruginosa. Mol Microbiol 110 (6): 995-1010. DOI: 10.1111/mmi.14132.
Mesrian DK, Purwaningtyas WE, Astuti RI, Hasan AEZ, Wahyudi AT. 2021. Methanol pigment extracts derived from two marine actinomycetes exhibit antibacterial and antioxidant activities. Biodiversitas 22 (10): 4440-4447. DOI: 10.13057/BIODIV/D221037.
Moayedi A, Nowroozi J, Sepahy AA. 2018. Cytotoxic effect of pyocyanin on human pancreatic cancer cell line (Panc-1). Iran J Basic Med Sci 21 (8): 794. DOI: 10.22038/IJBMS.2018.27865.6799.
Modolon F, Barno AR, Villela HDM, Peixoto RS. 2020. Ecological and biotechnological importance of secondary metabolites produced by coral?associated bacteria. J Appl Microbiol 129 (6): 1441-1457. DOI: 10.1111/jam.14766.
Mudaliar SB, Bharath Prasad AS. 2024. A biomedical perspective of pyocyanin from Pseudomonas aeruginosa: its applications and challenges. World J Microbiol Biotechnol 40 (3): 90. DOI: 10.1007/s11274-024-03889-0.
Narayani SS, Saranya P, Lokesh P, Ravindran J. 2021. Identification of bioactive compounds, characterization, optimization and cytotoxic study of pyocyanin against colon cancer cell line (HT-29). J Chem Pharm Res 13 (6): 1-18.
Nowroozi J, Sepahi AA, Rashnonejad A. 2012. Pyocyanine biosynthetic genes in clinical and environmental isolates of Pseudomonas aeruginosa and detection of pyocyanine’s antimicrobial effects with or without colloidal silver nanoparticles. Cell J 14 (1): 7-18.
Qiu S, Xu D, Xu M, Zhou H, Sun N, Zhang L, Wang W. 2022. Crystal structures of PigF, an O-methyltransferase involved in the prodigiosin synthetic pathway, reveal an induced-fit substrate-recognition mechanism. IUCrJ 9: 316-327. DOI: 10.1107/S2052252521011696.
Rante H, Alam G, Usmar U, Anwar RA, Ali A. 2022. Isolation of sponge bacterial symbionts from Kodingareng Keke Island-Makassar Indonesia which is potential as a producer of antimicrobial compounds. J Pure Appl Microbiol 16 (1): 737-744. DOI: 10.22207/JPAM.16.1.79.
Rini AF, Yuhana M, Wahyudi AT. 2017. Potency of sponge-associated bacteria producing bioactive compounds as biological control of vibriosis on shrimp. Jurnal Akuakultur Indonesia 16 (1): 41-50. DOI: 10.19027/jai.16.1.41-50.
Salam MA, Al-Amin MY, Salam MT, Pawar JS, Akhter N, Rabaan AA, Alqumber MA. 2023. Antimicrobial resistance: A growing serious threat for global public health. Healthcare 11 (13): 1946. DOI: 10.3390/healthcare11131946.
Sayed AM, Hassan MH, Alhadrami HA, Hassan HM, Goodfellow M, Rateb ME. 2020. Extreme environments: Microbiology leading to specialized metabolites. J Appl Microbiol 128 (3): 630-657. DOI: 10.1111/jam.14386.
Sholekha S, Budiarti S, Hasan AEZ, Krishanti NPRA,Wahyudi AT. 2024. Antimicrobial potential of an actinomycete Gordonia terrae JSN1. 9-derived orange pigment extract. Hayati 31 (1): 161-170. DOI: 10.4308/hjb.31.1.161-170.
Shouman H, Said HS, Kenawy HI, Hassan R. 2023. Molecular and biological characterization of pyocyanin from clinical and environmental Pseudomonas aeruginosa. Microb Cell Fact 22 (1): 166. DOI: 10.1186/s12934-023-02169-0.
Sullivan G, Spencer M. 2022. Heat and temperature. BJA education 22 (9): 350-356. DOI: 10.1016/j.bjae.2022.06.002.
Wahyudi AT, Nursari R, Purwaningtyas WE, Cahlia U, Priyanto JA. 2022. Crude extract of blue-green pigment derived from the marine bacterium Pseudomonas aeruginosa P1. S9 has antibacterial, antioxidant and cytotoxic Activities. Online J Biol Sci 22 (1): 118-25. DOI: 10.3844/ojbsci.2022.118.125.

Most read articles by the same author(s)

<< < 1 2 3 > >>