Optimization of Prodigiosin Production in Serratia marcescens: Effects of Growth Parameters on Antimicrobial and Cytotoxic Activities
Abstract
In this study, we isolated a red-colonial strain from marine soil collected in Colachel, Kanyakumari, Tamil Nadu, and identified it as Serratia marcescens via 16S rRNA sequencing. Optimization of various growth parameters was performed to increase pigment prodigiosin production. Mannitol was found to be an ideal carbon source with an optical density (OD) value of 1.99. A pH level (OD 1.92) and temperature of 27°C (OD 1.95) also promoted the favorable synthesis of pigment. Moreover, low salt concentration (0.5% NaCl) and a prolonged incubation period (120 h) significantly increased prodigiosin yield. It was found that higher prodigiosin production was achieved under shaking conditions (OD 2.25) than under static conditions (OD 1.12), and the pigment was maintained in methanol. The prodigiosin exhibited a strong antimicrobial effect against Staphylococcus aureus, with a zone of inhibition (ZOI) of 38 mm. The minimum inhibitory concentration (MIC) and the minimum bactericidal concentration (MBC) of the produced prodigiosin were 62.50 µg/mL. The index of 0.50 of the fractional inhibitory concentration (FIC) was an indication of the strong synergistic effect between prodigiosin and streptomycin. The pigment neutralized DPPH radicals and exhibited strong anticancer activity against MCF-7 breast cancer cells. This thorough study not only explains why optimizing the various growth parameters is important for maximizing prodigiosin synthesis but also examines their utility with respect to potency in both therapeutic and textile applications.
Keywords:
Anticancer, Antioxidant, Antimicrobial, Pigments, Serratia Marcescens
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References
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Chauhan, R., Choudhuri, A., & Abraham, J. (2017). Evaluation of antimicrobial, cytotoxicity, and dyeing properties of prodigiosin produced by Serratia marcescens strain JAR8. Asian Journal of Pharmaceutical and Clinical Research, 10, 279–283.
Choi, S. Y., Lim, S., Yoon, K. H., Lee, J. I., & Mitchell, R. J. (2021). Biotechnological activities and applications of bacterial pigments violacein and prodigiosin. Journal of Biological Engineering, 15, 1–6. https://doi.org/10.1186/s13036-021-00262-9
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Jaber, G. S., Dhaif, S. S., Hussian, T. A., Ibrahim, N. A., & Arifiyanto, A. (2023). Enhancing the prodigiosin pigment by adding Ag/TiO₂ synergism for antibacterial activity. Biocatalysis and Agricultural Biotechnology, 54, 102900. https://doi.org/10.1016/j.bcab.2023.102900
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Ma, Z., Xiao, H., Li, H., Lu, X., Yan, J., Nie, H., & Yin, Q. (2024). Prodigiosin as an antibiofilm agent against the bacterial biofilm-associated infection of Pseudomonas aeruginosa. Pathogens, 13(2), 145. https://doi.org/10.3390/pathogens13020145
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Mandal, R., Adhikari, A., Rana, G., & Mandal, T. (2017). Study of the useful characteristics of the red pigments of Serratia marcescens strains isolated from the soil. Journal of Applied Pharmaceutical Science, 7(8), 142–148. https://doi.org/10.7324/JAPS.2017.70820
Maurya, K. K., Tripathi, A. D., Kumar, D., & Srivastava, S. K. (2020). Production, purification, and characterization of prodigiosin by Serratia nematodiphilia using solid-state fermentation. Annals of Phytomedicine, 9, 302–306.
Mnif, S., Jardak, M., Bouizgarne, B., & Aifa, S. (2022). Prodigiosin from Serratia: Synthesis and potential applications. Asian Pacific Journal of Tropical Biomedicine, 12(6), 233–242.
Muslim, S. N., Mohammed Ali, A. N., & Alanisi, E. (2024). Anticancer and immunomodulatory activities of prodigiosin extracted and purified from Serratia marcescens. Asian Pacific Journal of Cancer Prevention, 25(9), 3051–3057.
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Nguyen, V. B., Wang, S. L., Nguyen, A. D., Phan, T. Q., Techato, K., & Pradit, S. (2021). Bioproduction of prodigiosin from fishery processing waste shrimp heads and evaluation of its potential bioactivities. Fishes, 6(3), 30. https://doi.org/10.3390/fishes6030030
Othman, M. A., El-Zamik, F. I., Hegazy, M. I., & Salama, A. S. (2019). Isolation and identification of Egyptian strains of Serratia marcescens producing antibacterial and antioxidant prodigiosin pigment. Zagazig Journal of Agricultural Research, 46(5), 1573–1582.
Pailliè-Jiménez, M. E., Stincone, P., & Brandelli, A. (2020). Natural pigments of microbial origin. Frontiers in Sustainable Food Systems, 4, 590439. https://doi.org/10.3389/fsufs.2020.590439
Paul, T., Bandyopadhyay, T. K., Mondal, A., Tiwari, O. N., Muthuraj, M., & Bhunia, B. (2020). A comprehensive review of recent trends in production, purification, and applications of prodigiosin. Biomass Conversion and Biorefinery. https://doi.org/10.1007/s13399-020-00928-2
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Pereira, R. F., & de Carvalho, C. C. (2024). Improving bioprocess conditions for the production of prodigiosin using a marine Serratia rubidaea strain. Marine Drugs, 22(4), 142. https://doi.org/10.3390/md22040142
Ramesh, C., Vinithkumar, N. V., Kirubagaran, R., Venil, C. K., & Dufossé, L. (2020). Applications of prodigiosin extracted from marine red-pigmented bacteria Zooshikella sp. and actinomycete Streptomyces sp. Microorganisms, 8(4), 556. https://doi.org/10.3390/microorganisms8040556
Renukadevi, K. P., & Vineeth, M. (2017). Antimicrobial, antioxidant and cytotoxicity activity of pigment produced from Serratia marcescens. European Journal of Biomedical and Pharmaceutical Sciences, 4(2), 265–269.
Sajjad, W., Din, G., Rafiq, M., Iqbal, A., Khan, S., Zada, S., Ali, B., & Kang, S. (2020). Pigment production by cold-adapted bacteria and fungi: A colorful tale of cryosphere with wide range applications. Extremophiles, 24, 447–473. https://doi.org/10.1007/s00792-020-01180-2
Sen, T., Barrow, C. J., & Deshmukh, S. K. (2019). Microbial pigments in the food industry—Challenges and the way forward. Frontiers in Nutrition, 6, 7. https://doi.org/10.3389/fnut.2019.00007
Srimathi, R., Priya, R., Nirmala, M., & Malarvizhi, A. (2017). Isolation, identification, optimization of prodigiosin pigment produced by Serratia marcescens and its applications. International Journal of Latest Engineering and Management Research, 2(9), 11–21.
Srilekha, V., Krishna, G., Sreelatha, B., Jagadeesh Kumar, E., & Rajeshwari, K. V. N. (2024). Prodigiosin: A fascinating and the most versatile bioactive pigment with diverse applications. Systems Microbiology and Biomanufacturing, 4(1), 66-76. https://doi.org/10.1007/s43393-023-00192-1
Sruthy, P. B., Anjana, J. C., Rathinamala, J., & Jayashree, S. (2014). The role of red pigment prodigiosin from bacteria of earthworm gut as an anticancer agent. Journal of Microbiology, Biotechnology and Food Sciences, 4(3), 246–251. https://doi.org/10.15414/jmbfs.2014-15.4.3.246-251
Sujitha, S., & Rajanarayanan, S. (2020). Isolation, characterization of Serratia marcescens from marine sediments and evaluation of potential biological applications. Journal of Advanced Scientific Research, 11, 51–59.
Sundararajan, P., & Ramasamy, S. P. (2024). Development of sustainable, eco-friendly antimicrobial finishing of cotton fabric using prodigiosin of Serratia marcescens SP1. Progress in Organic Coatings, 188, 108216. https://doi.org/10.1016/j.porgcoat.2024.108216
Swami, S. B., Ghgare, S. N., Swami, S. S., Shinde, K. J., Kalse, S. B., & Pardeshi, I. L. (2020). Natural pigments from plant sources: A review. The Pharma Innovation Journal, 9(10), 56–60.
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Balasubramaniam, B., Alexpandi, R., & Darjily, D. R. (2019). Exploration of the optimized parameters for bioactive prodigiosin mass production and its biomedical applications in vitro as well as in silico. Biocatalysis and Agricultural Biotechnology, 22, 101385. https://doi.org/10.1016/j.bcab.2019.101385
Chauhan, R., Choudhuri, A., & Abraham, J. (2017). Evaluation of antimicrobial, cytotoxicity, and dyeing properties of prodigiosin produced by Serratia marcescens strain JAR8. Asian Journal of Pharmaceutical and Clinical Research, 10, 279–283.
Choi, S. Y., Lim, S., Yoon, K. H., Lee, J. I., & Mitchell, R. J. (2021). Biotechnological activities and applications of bacterial pigments violacein and prodigiosin. Journal of Biological Engineering, 15, 1–6. https://doi.org/10.1186/s13036-021-00262-9
Darshan, N., & Manonmani, H. K. (2015). Prodigiosin and its potential applications. Journal of Food Science and Technology, 52, 5393–5407. https://doi.org/10.1007/s13197-015-1740-4
Dos Santos, R. A., Rodríguez, D. M., da Silva, L. A., de Almeida, S. M., de Campos-Takaki, G. M., & de Lima, M. A. (2021). Enhanced production of prodigiosin by Serratia marcescens UCP 1549 using agro substrates in solid-state fermentation. Archives of Microbiology, 203(7), 4091–4100. https://doi.org/10.1007/s00203-021-02399-z
Elkenawy, N. M., Yassin, A. S., Elhifnawy, H. N., & Amin, M. A. (2017). Optimization of prodigiosin production by Serratia marcescens using crude glycerol and enhancing production using gamma radiation. Biotechnology Reports, 14, 47–53. https://doi.org/10.1016/j.btre.2017.04.001
Formagio, A. S., Volobuff, C. R., Santiago, M., Cardoso, C. A., Vieira, M. D., & Pereira, Z. V. (2014). Evaluation of antioxidant activity, total flavonoids, tannins, and phenolic compounds in Psychotria leaf extracts. Antioxidants, 3(4), 745–757. https://doi.org/10.3390/antiox3040745
Fu, Q., Xiao, Y., Duan, X., Huang, H., Zhuang, Z., Shen, J., Pei, Y., Xu, H., & Gan, M. (2019). Continuous fermentation of a prodigiosin-producing Serratia marcescens strain isolated from soil. Advances in Bioscience and Biotechnology, 10(4), 98–108. https://doi.org/10.4236/abb.2019.104007
Garcha, S., Verma, N., & Brar, S. K. (2016). Isolation, characterization, and identification of microorganisms from unorganized dairy sector wastewater and sludge samples and evaluation of their biodegradability. Water Resources and Industry, 16, 19–28. https://doi.org/10.1016/j.wri.2016.10.002
Gohil, N., Bhattacharjee, G., & Singh, V. (2020). Synergistic bactericidal profiling of prodigiosin extracted from Serratia marcescens in combination with antibiotics against pathogenic bacteria. Microbial Pathogenesis, 149, 104508. https://doi.org/10.1016/j.micpath.2020.104508
Gondil, V. S., Asif, M., & Bhalla, T. C. (2017). Optimization of physicochemical parameters influencing the production of prodigiosin from Serratia nematodiphila RL2 and exploring its antibacterial activity. 3 Biotech, 7, 1–8. https://doi.org/10.1007/s13205-017-0979-z
Groeneveld, I., Kanelli, M., Ariese, F., & van Bommel, M. R. (2023). Parameters that affect the photodegradation of dyes and pigments in solution and on substrate—An overview. Dyes and Pigments, 210, 110999. https://doi.org/10.1016/j.dyepig.2022.110999
Gugu, T. H., Moses, I., Attama, K., Ibezim, E. C., Basarkar, G. D., & Patil, S. B. (2020). Optimized development, characterization, and antimicrobial evaluation of bioactive prodigiosin potentials from cephalosporin-resistant Serratia marcescens. Archives of Clinical Microbiology, 11(6), 130.
Guryanov, I., & Naumenko, E. (2024). Bacterial pigment prodigiosin as multifaceted compound for medical and industrial application. Applied Microbiology, 4(4), 1702–1728. https://doi.org/10.3390/applmicrobiol4040115
Hazarika, D. J., Kakoti, M., Kalita, R., Gautom#, T., Goswami, G., Barooah, M., & Boro, R. C. (2021). Prodigiosin from an endofungal bacterium Serratia marcescens D1 inhibits biofilm formation in gram-positive bacteria. Microbiology, 90(6), 829-838. https://doi.org/10.1134/S0026261722010052
Jaber, G. S., Dhaif, S. S., Hussian, T. A., Ibrahim, N. A., & Arifiyanto, A. (2023). Enhancing the prodigiosin pigment by adding Ag/TiO₂ synergism for antibacterial activity. Biocatalysis and Agricultural Biotechnology, 54, 102900. https://doi.org/10.1016/j.bcab.2023.102900
Ji, K., & Kim, Y. T. (2019). Antimicrobial activity of prodigiosin from Serratia sp. PDGS 120915 against intestinal pathogenic bacteria. Microbiology and Biotechnology Letters, 47(3), 459–464. https://doi.org/10.4014/mbl.1901.01006
Kumar, K., & Kumar, V. (2015). Prodigiosin alkaloids: Recent advancements in total synthesis and their biological potential. RSC Advances, 5(15), 10899–10920. https://doi.org/10.1039/C4RA10296G
Ma, Z., Xiao, H., Li, H., Lu, X., Yan, J., Nie, H., & Yin, Q. (2024). Prodigiosin as an antibiofilm agent against the bacterial biofilm-associated infection of Pseudomonas aeruginosa. Pathogens, 13(2), 145. https://doi.org/10.3390/pathogens13020145
Manas, N. H., Chong, L. Y., Tesfamariam, Y. M., Zulkharnain, A., Mahmud, H., Mahmod, D. S., Fuzi, S. F., & Azelee, N. I. (2020). Effects of oil substrate supplementation on production of prodigiosin by Serratia nematodiphila for dye-sensitized solar cell. Journal of Biotechnology, 317, 16–26. https://doi.org/10.1016/j.jbiotec.2020.04.011
Mandal, R., Adhikari, A., Rana, G., & Mandal, T. (2017). Study of the useful characteristics of the red pigments of Serratia marcescens strains isolated from the soil. Journal of Applied Pharmaceutical Science, 7(8), 142–148. https://doi.org/10.7324/JAPS.2017.70820
Maurya, K. K., Tripathi, A. D., Kumar, D., & Srivastava, S. K. (2020). Production, purification, and characterization of prodigiosin by Serratia nematodiphilia using solid-state fermentation. Annals of Phytomedicine, 9, 302–306.
Mnif, S., Jardak, M., Bouizgarne, B., & Aifa, S. (2022). Prodigiosin from Serratia: Synthesis and potential applications. Asian Pacific Journal of Tropical Biomedicine, 12(6), 233–242.
Muslim, S. N., Mohammed Ali, A. N., & Alanisi, E. (2024). Anticancer and immunomodulatory activities of prodigiosin extracted and purified from Serratia marcescens. Asian Pacific Journal of Cancer Prevention, 25(9), 3051–3057.
Nguyen, S. L., Nguyen, T. C., Do, T. T., Vu, T. L., Nguyen, T. T., Do, T. T., Nguyen, T. H., Le, T. H., Trinh, D. K., & Nguyen, T. A. (2022). Study on the anticancer activity of prodigiosin from variants of Serratia marcescens QBN VTCC 910026. BioMed Research International, 2022, 4053074. https://doi.org/10.1155/2022/4053074
Nguyen, V. B., Nguyen, D. N., & Wang, S. L. (2020). Microbial reclamation of chitin and protein-containing marine by-products for the production of prodigiosin and evaluation of its bioactivities. Polymers, 12(6), 1328. https://doi.org/10.3390/polym12061328
Nguyen, V. B., Wang, S. L., Nguyen, A. D., Phan, T. Q., Techato, K., & Pradit, S. (2021). Bioproduction of prodigiosin from fishery processing waste shrimp heads and evaluation of its potential bioactivities. Fishes, 6(3), 30. https://doi.org/10.3390/fishes6030030
Othman, M. A., El-Zamik, F. I., Hegazy, M. I., & Salama, A. S. (2019). Isolation and identification of Egyptian strains of Serratia marcescens producing antibacterial and antioxidant prodigiosin pigment. Zagazig Journal of Agricultural Research, 46(5), 1573–1582.
Pailliè-Jiménez, M. E., Stincone, P., & Brandelli, A. (2020). Natural pigments of microbial origin. Frontiers in Sustainable Food Systems, 4, 590439. https://doi.org/10.3389/fsufs.2020.590439
Paul, T., Bandyopadhyay, T. K., Mondal, A., Tiwari, O. N., Muthuraj, M., & Bhunia, B. (2020). A comprehensive review of recent trends in production, purification, and applications of prodigiosin. Biomass Conversion and Biorefinery. https://doi.org/10.1007/s13399-020-00928-2
Paul, T., Mondal, A., Bandyopadhyay, T. K., & Bhunia, B. (2024). Prodigiosin production and recovery from Serratia marcescens: Process development and cost-benefit analysis. Biomass Conversion and Biorefinery, 14(3), 4091–4110. https://doi.org/10.1007/s13399-022-02639-2
Pereira, R. F., & de Carvalho, C. C. (2024). Improving bioprocess conditions for the production of prodigiosin using a marine Serratia rubidaea strain. Marine Drugs, 22(4), 142. https://doi.org/10.3390/md22040142
Ramesh, C., Vinithkumar, N. V., Kirubagaran, R., Venil, C. K., & Dufossé, L. (2020). Applications of prodigiosin extracted from marine red-pigmented bacteria Zooshikella sp. and actinomycete Streptomyces sp. Microorganisms, 8(4), 556. https://doi.org/10.3390/microorganisms8040556
Renukadevi, K. P., & Vineeth, M. (2017). Antimicrobial, antioxidant and cytotoxicity activity of pigment produced from Serratia marcescens. European Journal of Biomedical and Pharmaceutical Sciences, 4(2), 265–269.
Sajjad, W., Din, G., Rafiq, M., Iqbal, A., Khan, S., Zada, S., Ali, B., & Kang, S. (2020). Pigment production by cold-adapted bacteria and fungi: A colorful tale of cryosphere with wide range applications. Extremophiles, 24, 447–473. https://doi.org/10.1007/s00792-020-01180-2
Sen, T., Barrow, C. J., & Deshmukh, S. K. (2019). Microbial pigments in the food industry—Challenges and the way forward. Frontiers in Nutrition, 6, 7. https://doi.org/10.3389/fnut.2019.00007
Srimathi, R., Priya, R., Nirmala, M., & Malarvizhi, A. (2017). Isolation, identification, optimization of prodigiosin pigment produced by Serratia marcescens and its applications. International Journal of Latest Engineering and Management Research, 2(9), 11–21.
Srilekha, V., Krishna, G., Sreelatha, B., Jagadeesh Kumar, E., & Rajeshwari, K. V. N. (2024). Prodigiosin: A fascinating and the most versatile bioactive pigment with diverse applications. Systems Microbiology and Biomanufacturing, 4(1), 66-76. https://doi.org/10.1007/s43393-023-00192-1
Sruthy, P. B., Anjana, J. C., Rathinamala, J., & Jayashree, S. (2014). The role of red pigment prodigiosin from bacteria of earthworm gut as an anticancer agent. Journal of Microbiology, Biotechnology and Food Sciences, 4(3), 246–251. https://doi.org/10.15414/jmbfs.2014-15.4.3.246-251
Sujitha, S., & Rajanarayanan, S. (2020). Isolation, characterization of Serratia marcescens from marine sediments and evaluation of potential biological applications. Journal of Advanced Scientific Research, 11, 51–59.
Sundararajan, P., & Ramasamy, S. P. (2024). Development of sustainable, eco-friendly antimicrobial finishing of cotton fabric using prodigiosin of Serratia marcescens SP1. Progress in Organic Coatings, 188, 108216. https://doi.org/10.1016/j.porgcoat.2024.108216
Swami, S. B., Ghgare, S. N., Swami, S. S., Shinde, K. J., Kalse, S. B., & Pardeshi, I. L. (2020). Natural pigments from plant sources: A review. The Pharma Innovation Journal, 9(10), 56–60.
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Anguraj, A. and Rathinasamy, S. (2026) “Optimization of Prodigiosin Production in Serratia marcescens: Effects of Growth Parameters on Antimicrobial and Cytotoxic Activities”, International Journal of Advancement in Life Sciences Research, 9(2), pp. 153-173. doi: https://doi.org/10.31632/ijalsr.2026.v09i02.012.
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