Fluoride-Induced Hormesis Enhances Cordycepin Production and Upregulates the Transcriptional Expression of its Biosynthesis Genes in Cordyceps militaris
Abstract
Cordyceps militaris is a medicinally valuable fungus known for producing cordycepin (3′-deoxyadenosine), a bioactive compound with anticancer, antioxidant, and immunomodulatory properties. However, its low natural yield limits large-scale commercial production. This study investigated the effects of fluoride-induced hormesis and growth supplements on cordycepin biosynthesis and the transcriptional regulation of key biosynthetic genes in C. militaris fruiting bodies. C. militaris strain 1164 was cultivated on rice-based substrate media supplemented with potassium fluoride (KF, 0.01–1 mM), glycine (500 mg/L), and ascorbic acid (100 mg/L). Cordycepin content was quantified using high-performance liquid chromatography (HPLC), while the expression of nine key genes (RNR, purA, purL, purB, PRPS, NT5E, purC, AMPD, and ADEK) was analyzed using quantitative real-time PCR (qRT-PCR). The results demonstrated that low-dose KF (0.01 mM) significantly enhanced cordycepin production, reaching 65.03 ± 0.73 mg/g dry weight (dwt.), which represents a 69.93% increase compared with the control (38.6 ± 0.15 mg/g dwt.). Glycine and ascorbic acid supplementation also increased cordycepin content to 48.16 ± 0.25 and 61.36 ± 0.41 mg/g dwt., respectively. Gene expression analysis revealed a dose-dependent response, with 0.1 mM KF strongly upregulating purA (6.92-fold), PRPS (4.75-fold), and RNR (3.76-fold). In contrast, 1 mM KF suppressed both gene expression and fungal growth. Glycine and ascorbic acid notably increased RNR expression by 2.5-fold and 2.3-fold, respectively, consistent with the observed enhancement in cordycepin production. This study is the first to demonstrate fluoride-induced hormetic regulation of cordycepin biosynthetic genes. The findings indicate that low-dose KF functions as a metabolic and transcriptional enhancer, providing a novel strategy for optimizing cordycepin production in C. militaris through targeted supplementation approaches.
Keywords:
Cordyceps militaris, Cordycepin, Fluoride, Transcriptional Expression
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References
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Chang, Y., Liu, X., Jiao, Y., & Zheng, X. (2024). Improved cordycepin production by Cordyceps militaris using corn steep liquor hydrolysate as an alternative protein nitrogen source. Foods, 13(5), 813. https://doi.org/10.3390/foods13050813
Chen, Y. (2003). Differences in fluoride effects on fecundity among varieties of the silkworm Bombyx mori. Fluoride, 36(3), 163-169. https://www.fluorideresearch.org/363/files/FJ2003_v36_n3_p163-169.pdf
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Hou, S. J., Cheng, K. C., Lin, S. H., Hsiao, I. L., Santoso, S. P., Singajaya, S., ... & Lin, S. P. (2024). Improvement of extracellular polysaccharides production from Cordyceps militaris immobilized alginate beads in repeated-batch fermentation. Lwt, 193, 115752. https://doi.org/10.1016/j.lwt.2024.115752
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In-On, A., Thananusak, R., Ruengjitchatchawalya, M., Vongsangnak, W., & Laomettachit, T. (2022). Construction of light-responsive gene regulatory network for growth, development and secondary metabolite production in Cordyceps militaris. Biology, 11(1), 71. https://doi.org/10.3390/biology11010071
Ismailhodjaev, B., Mirzaqobulov, J., Kholmirzaeva, B., Kuatbekova, K., Eskaraev, N., & Abduraimova, N. (2022, June). Comparative study of the activity and localization of carbonic anhydrase in some microalgae and their dependence on the concentration of carbon dioxide and nitrogen supply. In AIP Conference Proceedings (Vol. 2432, No. 1, p. 050066). AIP Publishing LLC. https://doi.org/10.1063/12.0015245
Jarosz, Z., & Pitura, K. (2021). Fluoride toxicity limit—can the element exert a positive effect on plants?. Sustainability, 13(21), 12065. https://doi.org/10.3390/su132112065
Jędrejko, K. J., Lazur, J., & Muszyńska, B. (2021). Cordyceps militaris: An overview of its chemical constituents in relation to biological activity. Foods, 10(11), 2634. https://doi.org/10.3390/foods10112634
Jeennor, S., Anantayanon, J., Panchanawaporn, S., Chutrakul, C., Vongsangnak, W., & Laoteng, K. (2023). Efficient de novo production of bioactive cordycepin by Aspergillus oryzae using a food-grade expression platform. Microbial Cell Factories, 22(1), 253. https://doi.org/10.1186/s12934-023-02261-5
Kaewkod, T., Ngamsaoad, P., Mayer, K. O., Cheepchirasuk, N., Promputtha, I., & Tragoolpua, Y. (2024). Antioxidant, Antibacteria, and Anti‐Inflammatory Effects of Cordyceps militaris Extracts and Their Bioactive Compounds. Journal of Food Biochemistry, 2024(1), 1862818. https://doi.org/10.1155/jfbc/1862818
Kaushik, V., Singh, A., Arya, A., Sindhu, S. C., Sindhu, A., & Singh, A. (2020). Enhanced production of cordycepin in Ophiocordyceps sinensis using growth supplements under submerged conditions. Biotechnology Reports, 28, e00557. https://doi.org/10.1016/j.btre.2020.e00557
Kulcsár, S., Turbók, J., Kövér, G., Balogh, K., Zándoki, E., Ali, O., ... & Mézes, M. (2024). Exposure to a combination of fusarium mycotoxins leads to lipid peroxidation and influences antioxidant defenses, fatty acid composition of phospholipids, and renal histology in laying hens. Toxins, 16(5), 226. https://doi.org/10.3390/toxins16050226
Kunhorm, P., Chueaphromsri, P., Chaicharoenaudomrung, N., & Noisa, P. (2022). Enhancement of cordycepin production from Cordyceps militaris culture by epigenetic modification. Biotechnology letters, 44(4), 581-593. https://doi.org/10.1007/s10529-022-03241-2
Li, W., Zhao, B., Liu, X., He, Z., Xie, L., & Qian, Z. (2025). Purification, structural characterization, and in vitro immunomodulatory activity of a low-molecular-weight polysaccharide from cultivated Chinese cordyceps. International Journal of Biological Macromolecules, 301, 140394. https://doi.org/10.1016/j.ijbiomac.2025.140394
Li, X., Jiang, R., Wang, S., Li, C., Xu, Y., Li, S., ... & Wang, L. (2024). Prospects for cordycepin biosynthesis in microbial cell factories. Frontiers in Chemical Engineering, 6, 1446454. https://doi.org/10.3389/fceng.2024.1446454
Li, X., Wang, J., Zhang, H., Xiao, L., Lei, Z., Kaul, S. C., ... & Zhang, Z. (2021). Low dose of fluoride in the culture medium of Cordyceps militaris promotes its growth and enhances bioactives with antioxidant and anticancer properties. Journal of fungi, 7(5), 342. https://doi.org/10.3390/jof7050342
Lusakunwiwat, P., Thananusak, R., Nopgason, R., Laoteng, K., & Vongsangnak, W. (2024). Holistic transcriptional responses of Cordyceps militaris to different culture temperatures. Gene, 923, 148574. https://doi.org/10.1016/j.gene.2024.148574
Peng, T., Guo, J., & Tong, X. (2024). Advances in biosynthesis and metabolic engineering strategies of cordycepin. Frontiers in Microbiology, 15, 1386855. https://doi.org/10.3389/fmicb.2024.1386855
Rajak, P., Roy, S., Khatun, S., Mandi, M., Ganguly, A., Das, K., ... & Biswas, G. (2023). Fluoride contamination, toxicity and its potential therapeutic agents. Toxicology International, 29(4), 553-565. https://doi:10.18311/ti/2022/v29i4/30844
Shweta., Abdullah, S., Komal., & Kumar, A. (2023). A brief review on the medicinal uses of Cordyceps militaris. Pharmacological Research - Modern Chinese Medicine, 7, 100228. https://doi.org/10.1016/j.prmcm.2023.100228
Wang, L., Yan, H., Zeng, B., & Hu, Z. (2022). Research progress on cordycepin synthesis and methods for enhancement of cordycepin production in Cordyceps militaris. Bioengineering, 9(2), 69. https://doi.org/10.3390/bioengineering9020069
Wang, X., Li, Y., Li, X., Sun, L., Feng, Y., Sa, F., ... & Cheng, X. (2023). Transcriptome and metabolome profiling unveils the mechanisms of naphthalene acetic acid in promoting cordycepin synthesis in Cordyceps militaris. Frontiers in Nutrition, 10, 1104446. https://doi.org/10.3389/fnut.2023.1104446
Werapan, B., Nutaratat, P., Ariyaphuttarat, S., & Prathumpai, W. (2022). Cordycepin production by the potential fungal strains Cordyceps militaris BCC 2819 and Cordyceps cicadae BCC 19788 in submerged culture during batch and fed-batch fermentation. African Journal of Biotechnology, 21(10), 483-503. https://doi.org/10.5897/AJB2022.17514
Xie, J., Wang, J., Wang, X., Chen, M., Yao, B., Dong, Y., ... & Wu, Y. (2023). An engineered dermal substitute with mesenchymal stem cells enhances cutaneous wound healing. Tissue Engineering Part A, 29(17-18), 491-505. https://doi.org/10.1089/ten.tea.2023.0071
Yang, Y., Huang, J., Dong, G., & Hu, X. (2025). Telomere-to-Telomere Assembly of the Cordyceps militaris CH1 Genome and Integrated Transcriptomic and Metabolomic Analyses Provide New Insights into Cordycepin Biosynthesis Under Light Stress. Journal of Fungi, 11(6), 461. https://doi.org/10.3390/jof11060461
Yoo, C. H., Sadat, M. A., Kim, W., Park, T. S., Park, D. K., & Choi, J. (2022). Comprehensive transcriptomic analysis of Cordyceps militaris cultivated on germinated soybeans. Mycobiology, 50(1), 1-11. https://doi.org/10.1080/12298093.2022.2035906
Yu, L., Zhao, J., Li, S. P., Fan, H., Hong, M., Wang, Y. T., & Zhu, Q. (2006). Quality evaluation of Cordyceps through simultaneous determination of eleven nucleosides and bases by RP‐HPLC. Journal of Separation science, 29(7), 953-958. https://doi.org/10.1002/jssc.200600007
Zeng, J., Zhou, Y., Lyu, M., Huang, X., Xie, M., Huang, M., ... & Wei, T. (2024). Cordyceps militaris: A novel mushroom platform for metabolic engineering. Biotechnology Advances, 74, 108396. https://doi.org/10.1016/j.biotechadv.2024.108396
Zhang, F. L., Yang, X. F., Wang, D., Lei, S. R., Guo, L. A., Liu, W. J., & Song, J. (2020). A simple and effective method to discern the true commercial Chinese cordyceps from counterfeits. Scientific Reports, 10(1), 2974. https://doi:10.1038/s41598-020-59900-9
Zhang, H., Yu-Xian, Wang, Y. X., Tong, X. X. Yokoyama, W., Cao, J., Wang, F., Peng, C., & Guo, J. L. (2020). Overexpression of ribonucleotide reductase small subunit, RNRM, increases cordycepin biosynthesis in transformed Cordyceps militaris. Chinese Journal of Natural Medicines, 18(5), 393-400. https://doi.org/10.1016/S1875-5364(20)30046-7
Zhao, B., Ding, H., Hu, T., & Guo, Y. (2023). Synergistic effects of the Se and Zn supplemental combination on the nutrient improvement of mannitol and adenosine and the multi-element bioaccessibility in Cordyceps cicadae. LWT, 173, 114354. https://doi.org/10.1016/j.lwt.2022.114354
Zhu, Z., Xiang, Y., Yan, X., Shi, C., Chen, C., Liu, H., ... & Wu, D. (2025). Stable cross-linked polyacrylamide stationary phase based on atom transfer radical polymerization for hydrophilic interaction liquid chromatography. Microchemical Journal, 213, 113818. https://doi.org/10.1016/j.microc.2025.113818
Borde, M., & Singh, S. K. (2023). Enhanced production of cordycepin under solid-state fermentation of Cordyceps militaris by using combinations of grains/substrates. Brazilian Journal of Microbiology, 54(4), 2765-2772. https://doi.org/10.1007/s42770-023-01169-x
Buradam, P., Thananusak, R., Koffas, M., Chumnanpuen, P., & Vongsangnak, W. (2024). Expanded Gene Regulatory Network Reveals Potential Light-Responsive Transcription Factors and Target Genes in Cordyceps militaris. International Journal of Molecular Sciences, 25(19), 10516. https://doi.org/10.3390/ijms251910516
Burgstahler, A. W. (2002). Paradoxical dose-response effects of fluoride. Fluoride, 35(143), e147. https://hero.epa.gov/reference/2054892/
Chang, Y., Liu, X., Jiao, Y., & Zheng, X. (2024). Improved cordycepin production by Cordyceps militaris using corn steep liquor hydrolysate as an alternative protein nitrogen source. Foods, 13(5), 813. https://doi.org/10.3390/foods13050813
Chen, Y. (2003). Differences in fluoride effects on fecundity among varieties of the silkworm Bombyx mori. Fluoride, 36(3), 163-169. https://www.fluorideresearch.org/363/files/FJ2003_v36_n3_p163-169.pdf
Doley, D. (1989). Fluoride‐induced enhancement and inhibition of shoot growth in four taxa of Pinus. New Phytologist, 112(4), 543-552. https://doi.org/10.1111/j.1469-8137.1989.tb00349.x
Hou, S. J., Cheng, K. C., Lin, S. H., Hsiao, I. L., Santoso, S. P., Singajaya, S., ... & Lin, S. P. (2024). Improvement of extracellular polysaccharides production from Cordyceps militaris immobilized alginate beads in repeated-batch fermentation. Lwt, 193, 115752. https://doi.org/10.1016/j.lwt.2024.115752
Hu, Y., Wu, Y., Song, J., Ma, M., Xiao, Y., & Zeng, B. (2024). Advancing Cordyceps militaris Industry: Gene Manipulation and Sustainable Biotechnological Strategies. Bioengineering, 11(8), 783. https://doi.org/10.3390/bioengineering11080783
In-On, A., Thananusak, R., Ruengjitchatchawalya, M., Vongsangnak, W., & Laomettachit, T. (2022). Construction of light-responsive gene regulatory network for growth, development and secondary metabolite production in Cordyceps militaris. Biology, 11(1), 71. https://doi.org/10.3390/biology11010071
Ismailhodjaev, B., Mirzaqobulov, J., Kholmirzaeva, B., Kuatbekova, K., Eskaraev, N., & Abduraimova, N. (2022, June). Comparative study of the activity and localization of carbonic anhydrase in some microalgae and their dependence on the concentration of carbon dioxide and nitrogen supply. In AIP Conference Proceedings (Vol. 2432, No. 1, p. 050066). AIP Publishing LLC. https://doi.org/10.1063/12.0015245
Jarosz, Z., & Pitura, K. (2021). Fluoride toxicity limit—can the element exert a positive effect on plants?. Sustainability, 13(21), 12065. https://doi.org/10.3390/su132112065
Jędrejko, K. J., Lazur, J., & Muszyńska, B. (2021). Cordyceps militaris: An overview of its chemical constituents in relation to biological activity. Foods, 10(11), 2634. https://doi.org/10.3390/foods10112634
Jeennor, S., Anantayanon, J., Panchanawaporn, S., Chutrakul, C., Vongsangnak, W., & Laoteng, K. (2023). Efficient de novo production of bioactive cordycepin by Aspergillus oryzae using a food-grade expression platform. Microbial Cell Factories, 22(1), 253. https://doi.org/10.1186/s12934-023-02261-5
Kaewkod, T., Ngamsaoad, P., Mayer, K. O., Cheepchirasuk, N., Promputtha, I., & Tragoolpua, Y. (2024). Antioxidant, Antibacteria, and Anti‐Inflammatory Effects of Cordyceps militaris Extracts and Their Bioactive Compounds. Journal of Food Biochemistry, 2024(1), 1862818. https://doi.org/10.1155/jfbc/1862818
Kaushik, V., Singh, A., Arya, A., Sindhu, S. C., Sindhu, A., & Singh, A. (2020). Enhanced production of cordycepin in Ophiocordyceps sinensis using growth supplements under submerged conditions. Biotechnology Reports, 28, e00557. https://doi.org/10.1016/j.btre.2020.e00557
Kulcsár, S., Turbók, J., Kövér, G., Balogh, K., Zándoki, E., Ali, O., ... & Mézes, M. (2024). Exposure to a combination of fusarium mycotoxins leads to lipid peroxidation and influences antioxidant defenses, fatty acid composition of phospholipids, and renal histology in laying hens. Toxins, 16(5), 226. https://doi.org/10.3390/toxins16050226
Kunhorm, P., Chueaphromsri, P., Chaicharoenaudomrung, N., & Noisa, P. (2022). Enhancement of cordycepin production from Cordyceps militaris culture by epigenetic modification. Biotechnology letters, 44(4), 581-593. https://doi.org/10.1007/s10529-022-03241-2
Li, W., Zhao, B., Liu, X., He, Z., Xie, L., & Qian, Z. (2025). Purification, structural characterization, and in vitro immunomodulatory activity of a low-molecular-weight polysaccharide from cultivated Chinese cordyceps. International Journal of Biological Macromolecules, 301, 140394. https://doi.org/10.1016/j.ijbiomac.2025.140394
Li, X., Jiang, R., Wang, S., Li, C., Xu, Y., Li, S., ... & Wang, L. (2024). Prospects for cordycepin biosynthesis in microbial cell factories. Frontiers in Chemical Engineering, 6, 1446454. https://doi.org/10.3389/fceng.2024.1446454
Li, X., Wang, J., Zhang, H., Xiao, L., Lei, Z., Kaul, S. C., ... & Zhang, Z. (2021). Low dose of fluoride in the culture medium of Cordyceps militaris promotes its growth and enhances bioactives with antioxidant and anticancer properties. Journal of fungi, 7(5), 342. https://doi.org/10.3390/jof7050342
Lusakunwiwat, P., Thananusak, R., Nopgason, R., Laoteng, K., & Vongsangnak, W. (2024). Holistic transcriptional responses of Cordyceps militaris to different culture temperatures. Gene, 923, 148574. https://doi.org/10.1016/j.gene.2024.148574
Peng, T., Guo, J., & Tong, X. (2024). Advances in biosynthesis and metabolic engineering strategies of cordycepin. Frontiers in Microbiology, 15, 1386855. https://doi.org/10.3389/fmicb.2024.1386855
Rajak, P., Roy, S., Khatun, S., Mandi, M., Ganguly, A., Das, K., ... & Biswas, G. (2023). Fluoride contamination, toxicity and its potential therapeutic agents. Toxicology International, 29(4), 553-565. https://doi:10.18311/ti/2022/v29i4/30844
Shweta., Abdullah, S., Komal., & Kumar, A. (2023). A brief review on the medicinal uses of Cordyceps militaris. Pharmacological Research - Modern Chinese Medicine, 7, 100228. https://doi.org/10.1016/j.prmcm.2023.100228
Wang, L., Yan, H., Zeng, B., & Hu, Z. (2022). Research progress on cordycepin synthesis and methods for enhancement of cordycepin production in Cordyceps militaris. Bioengineering, 9(2), 69. https://doi.org/10.3390/bioengineering9020069
Wang, X., Li, Y., Li, X., Sun, L., Feng, Y., Sa, F., ... & Cheng, X. (2023). Transcriptome and metabolome profiling unveils the mechanisms of naphthalene acetic acid in promoting cordycepin synthesis in Cordyceps militaris. Frontiers in Nutrition, 10, 1104446. https://doi.org/10.3389/fnut.2023.1104446
Werapan, B., Nutaratat, P., Ariyaphuttarat, S., & Prathumpai, W. (2022). Cordycepin production by the potential fungal strains Cordyceps militaris BCC 2819 and Cordyceps cicadae BCC 19788 in submerged culture during batch and fed-batch fermentation. African Journal of Biotechnology, 21(10), 483-503. https://doi.org/10.5897/AJB2022.17514
Xie, J., Wang, J., Wang, X., Chen, M., Yao, B., Dong, Y., ... & Wu, Y. (2023). An engineered dermal substitute with mesenchymal stem cells enhances cutaneous wound healing. Tissue Engineering Part A, 29(17-18), 491-505. https://doi.org/10.1089/ten.tea.2023.0071
Yang, Y., Huang, J., Dong, G., & Hu, X. (2025). Telomere-to-Telomere Assembly of the Cordyceps militaris CH1 Genome and Integrated Transcriptomic and Metabolomic Analyses Provide New Insights into Cordycepin Biosynthesis Under Light Stress. Journal of Fungi, 11(6), 461. https://doi.org/10.3390/jof11060461
Yoo, C. H., Sadat, M. A., Kim, W., Park, T. S., Park, D. K., & Choi, J. (2022). Comprehensive transcriptomic analysis of Cordyceps militaris cultivated on germinated soybeans. Mycobiology, 50(1), 1-11. https://doi.org/10.1080/12298093.2022.2035906
Yu, L., Zhao, J., Li, S. P., Fan, H., Hong, M., Wang, Y. T., & Zhu, Q. (2006). Quality evaluation of Cordyceps through simultaneous determination of eleven nucleosides and bases by RP‐HPLC. Journal of Separation science, 29(7), 953-958. https://doi.org/10.1002/jssc.200600007
Zeng, J., Zhou, Y., Lyu, M., Huang, X., Xie, M., Huang, M., ... & Wei, T. (2024). Cordyceps militaris: A novel mushroom platform for metabolic engineering. Biotechnology Advances, 74, 108396. https://doi.org/10.1016/j.biotechadv.2024.108396
Zhang, F. L., Yang, X. F., Wang, D., Lei, S. R., Guo, L. A., Liu, W. J., & Song, J. (2020). A simple and effective method to discern the true commercial Chinese cordyceps from counterfeits. Scientific Reports, 10(1), 2974. https://doi:10.1038/s41598-020-59900-9
Zhang, H., Yu-Xian, Wang, Y. X., Tong, X. X. Yokoyama, W., Cao, J., Wang, F., Peng, C., & Guo, J. L. (2020). Overexpression of ribonucleotide reductase small subunit, RNRM, increases cordycepin biosynthesis in transformed Cordyceps militaris. Chinese Journal of Natural Medicines, 18(5), 393-400. https://doi.org/10.1016/S1875-5364(20)30046-7
Zhao, B., Ding, H., Hu, T., & Guo, Y. (2023). Synergistic effects of the Se and Zn supplemental combination on the nutrient improvement of mannitol and adenosine and the multi-element bioaccessibility in Cordyceps cicadae. LWT, 173, 114354. https://doi.org/10.1016/j.lwt.2022.114354
Zhu, Z., Xiang, Y., Yan, X., Shi, C., Chen, C., Liu, H., ... & Wu, D. (2025). Stable cross-linked polyacrylamide stationary phase based on atom transfer radical polymerization for hydrophilic interaction liquid chromatography. Microchemical Journal, 213, 113818. https://doi.org/10.1016/j.microc.2025.113818
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Singh, P., Joshi, R., Bulakarima, H., Yadav, A., & Shehu, I. (2026). Fluoride-Induced Hormesis Enhances Cordycepin Production and Upregulates the Transcriptional Expression of its Biosynthesis Genes in Cordyceps militaris. International Journal of Advancement in Life Sciences Research, 9(1), 117-128. https://doi.org/https://doi.org/10.31632/ijalsr.2026.v09i01.009
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