Fibrinolytic Protease Activity of Crude Enzyme from Fermented Sunflower (Helianthus annuus) and Common Bean (Phaseolus vulgaris) seeds by Rhizopus microsporus var. oligosporus FNCC 6010 in Solid State Fermentation
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Submitted
28 January 2023
Published
30 August 2023
Keywords:
-
Fibrinolytic, Helianthus annuus L., Phaseolus vulgaris L., Rhizopus microsporus var. oligosporus, Protease
Abstract
In the entire world, cardiovascular diseases (CVDs) are the main cause of death. For the treatment of CVDs, microbial fibrinolytic enzymes are highly regarded as novel therapeutic candidates. This study was purposed to determine the fibrinolytic protease activity produced by fungus source, which is Rhizopus microsporus var. oligosporus FNCC 6010 in fermented sunflower (Helianthus annuus) seed and common bean (Phaseolus vulgaris) seed. Fermentation was carried out by solid-state fermentation method at an initial pH of 5, incubation temperature of 33±1°C, and incubation time of 24 hours. The fermented seed was extracted to obtain supernatant as the crude enzyme. The proteolytic activity assay was done by the skimmed milk agar (SMA) plate method to obtain the proteolytic index, and the fibrinolytic activity assay was conducted by the fibrin-agarose plate method to get the fibrinolytic index. The results show that crude enzymes from fermented H. annuus and P. vulgaris seeds by R. microsporus have fibrinolytic protease activity with proteolytic index 2.64 ± 0.01 and 2.23 ± 0.04, respectively. The fibrinolytic index is 2.40 ± 0.06 and 1.64 ± 0.06, respectively. Therefore, the crude enzyme has the potential to be further researched as a candidate for thrombolytic agents. The purification, characterization, and in-depth research are needed to develop enzymes into preparations for preventing and treating CVDs.
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References
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19. Srivastava N, Srivastava M, Ramteke W, Mishra K. Chapter 23 - Solid-State Fermentation Strategy for Microbial Metabolites Production: An Overview. In: Gupta VK, Pandey A, editors. New and Future Developments in Microbial Biotechnology and Bioengineering: Microbial Secondary Metabolites Biochemistry and Applications. Amsterdam: Elsevier; 2019. p. 345-54. doi:10.1016/B978-0-444-63504-4.00023-2
20. Ahamed NA, Arif IA, Al-rashed S, Panneerselvam A, Ambikapathy V. In vitro thrombolytic potential of fibrinolytic enzyme from Brevibacterium sp. isolated from the root of the plant, Aloe castellorum. J King Saud Univ Sci. 2022;34(3):101868. doi:10.1016/j.jksus.2022.101868
21. Jo C, Zhang J, Tam JM, Church GM, Khalil AM, Segrè D, et al. Unlocking the magic in mycelium: Using synthetic biology to optimize filamentous fungi for biomanufacturing and sustainability. Mater Today Bio. 2023;19:100560. doi:10.1016/j.mtbio.2023.100560
22. Hermansyah B, Lokapirnasari WP. Pengaruh Subtitusi Tepung Biji Bunga Matahari (Helianthus Annuus L.) dalam Pakan Komersial dengan Konsentrasi Tertentu Terhadap Performa Ayam Pedaging. J Med Vet. 2019;2(1):7-12. doi:10.20473/jmv.vol2.iss1.2019.7-12
23. Lakshmi NJ, Vanaja M, Yadav SK, Maheswari M, Archana G, Patil A, et al. Effect of CO2 on growth, seed yield and nitrogen uptake in sunflower. J Agrometeorol. 2017;19(3):195-9. doi:10.54386/jam.v19i3.620
24. Franco R, Iseppi L, Taverna M. Sunflower Oil Functional Properties for Specialty Food. Nutr Food Sci Int J. 2018;5(4):4-7. doi:10.19080/nfsij.2018.05.555668
25. Karefyllakis D, van der Goot AJ, Nikiforidis CV. Multicomponent emulsifiers from sunflower seeds. Curr Opin Food Sci. 2019;29:35-41. doi:10.1016/j.cofs.2019.07.005
26. Grasso S, Pintado T, Pérez-Jiménez J, Ruiz-Capillas C, Herrero AM. Potential of a sunflower seed by-product as animal fat replacer in healthier frankfurters. Foods. 2020;9(4):445. doi:10.3390/foods9040445
27. Özacar M, Mehde AA, Mehdi WA, Özacar ZZ, Severgün O. The novel multi cross-linked enzyme aggregates of protease, lipase, and catalase production from the sunflower seeds, characterization and application. Colloids Surf B Biointerfaces. 2019;173:58-68. doi:10.1016/j.colsurfb.2018.09.042
28. Rauf A, Irfan M, Nadeem M, Ahmed I, Iqbal HMN. Optimization of Growth Conditions for Acidic Protease Production from Rhizopus oligosporus through Solid State Fermentation of Sunflower Meal. Int J Biotechnol Bioeng. 2010;4(12):898-901. doi:10.5281/zenodo.1079814
29. Celmeli T, Sari H. The Nutritional Content of Common Bean (Phaseolus vulgaris L.) Landraces in Comparison to Modern Varieties. Agronomy. 2018;8(9):166. doi:10.3390/agronomy8090166
30. Rodríguez L, Mendez D, Montecino H, Carrasco B, Arevalo B, Palomo I, et al. Role of Phaseolus vulgaris L. in the Prevention of Cardiovascular Diseases-Cardioprotective Potential of Bioactive Compounds. Plants. 2022;11(2):186. doi:10.3390/plants11020186
31. Chávez-Mendoza C, Hernández-Figueroa KI, Sánchez E. Antioxidant capacity and phytonutrient content in the seed coat and cotyledon of common beans (Phaseolus vulgaris L.) from various regions in Mexico. Antioxidants. 2019;8(1):5. doi:10.3390/antiox8010005
32. Poernomo AT, Isnaeni, Purwanto. Aktivitas Invitro Enzim Fibrinolitik Ekstrak Tempe Hasil Fermentasi Rhizopus Oligosporus ATCC 6010 Pada Substrat Kedelai Hitam. Berkala Ilmiah Kimia Farmasi. 2015;4(2):19-26.
33. Sambo S, Magashi AM, Farouq AA, Hassan SW. An overview of the solid state fermentation in the production of fungal protease enzymes. World J Adv Res Rev. 2021;9(3):85-9. doi:10.30574/wjarr.2021.9.3.0061
34. Susanti E, Lutfiana N, Suharti, Retnosari R. Screening of proteolytic bacteria from tauco Surabaya based on pathogenicity and selectivity of its protease on milky fish (Chanos chanos) scales for healthy and halal collagen production. IOP Conf Ser Mater Sci Eng. 2019;509:012044. doi:10.1088/1757-899X/509/1/012044
35. Muisristanto D, Poernomo AT, Sugijanto. Isolasi dan Penapisan Fibrinolitik Jamur Tanah Hutan Mangrove Wonorejo Surabaya. Berkala Ilmiah Kimia Farmasi. 2015;4(2):11-7.
36. Handoyo T, Morita N. Structural and Functional Properties of Fermented Soybean (Tempeh) by Using Rhizopus oligosporus. Int J Food Prop. 2006;9(2)347-55. doi:10.1080/10942910500224746
37. Upgade A, Nandeshwar A, Samant L. Assessment of fungal protease enzyme from French bean using A. niger by Solid State Fermentation. J Microbiol Biotechnol Res. 2011;1(4):45-51.
38. Raju EVN, Divakar G. An Overview on microbial fibrinolytic proteases. Int J Pharm Sci Res. 2014;5(3):643-56. doi:10.13040/IJPSR.0975-8232.5(3).643-56
39. Rashad MM, Mahmoud AE, Al-Kashef AS, Nooman MU. Purification and characterization of a novel fibrinolytic enzyme by Candida guilliermondii grown on sunflower oil cake. J Appl Sci Res. 2012;8(2):635-45.
40. Akhtar T, Hoq M, Mazid A. Bacterial Proteases as Thrombolytics and Fibrinolytics. Dhaka Univ J Pharm Sci. 2017;16(2):255-69. doi:10.3329/dujps.v16i2.35265
41. Gond SP, Sharma RA. Agro Waste Mediated Production of Fibrinolytic Enzyme and Its Optimization and Application. Int J Sci Res. 2022;11(2):58-63. doi:10.21275/SR22130105418
2. Kotb E. Purification and partial characterization of serine fibrinolytic enzyme from Bacillus megaterium KSK-07 isolated from kishk, a traditional Egyptian fermented food. Appl Biochem Microbiol. 2015;51:34-43. doi:10.1134/S000368381501007X
3. Dhillon A, Sharma K, Rajulapati V, Goyal A. 7 - Proteolytic Enzymes. In: Pandey A, Negi S, Soccol CR, editors. Current Developments in Biotechnology and Bioengineering: Production, Isolation and Purification of Industrial Products. Amsterdam: Elsevier; 2017. p. 149-73. doi:10.1016/B978-0-444-63662-1.00007-5
4. Kotb E. Activity assessment of microbial fibrinolytic enzymes. Appl Microbiol Biotechnol. 2013;97(15):6647-65. doi:10.1007/s00253-013-5052-1
5. Sharma C, Osmolovskiy A, Singh R. Microbial fibrinolytic enzymes as anti-thrombotics: Production, characterisation and prodigious biopharmaceutical applications. Pharmaceutics. 2021;13(11):1880. doi:10.3390/pharmaceutics13111880
6. Rajaselvam J, Benit N, Alotaibi SS, Rathi MA, Srigopalram S, Biji GD, et al. In vitro fibrinolytic activity of an enzyme purified from Bacillus amyloliquefaciens strain KJ10 isolated from soybean paste. Saudi J Biol Sci. 2021;28(8):4117-23. doi:10.1016/j.sjbs.2021.04.061
7. Yogesh D, Halami PM. Fibrinolytic enzymes of Bacillus spp.: An overview. Int Food Res J. 2017;24(1):35-47.
8. Stephani L, Tjandrawinata RR, Afifah DN, Lim Y, Ismaya WT, Suhartono MT. Food Origin Fibrinolytic Enzyme with Multiple Actions. HAYATI J Biosci. 2017;24(3):124-30. doi:10.1016/j.hjb.2017.09.003
9. Sada A, Sugianto NE, Poernomo AT. Produksi Enzim Fibrinolitik Tempe oleh Rhizopus oryzae FNCC 6078. Berkala Ilmiah Kimia Farmasi. 2021;8(1):1-6. doi:10.20473/bikfar.v8i1.31202
10. Xiao-Lan L, Lian-Xiang D, Fu-Ping L, Xi-Qun Z, Jing X. Purification and characterization of a novel fibrinolytic enzyme from Rhizopus chinensis 12. Appl Microbiol Biotechnol. 2005;67(2):209-14. doi:10.1007/s00253-004-1846-5
11. Wei X, Luo M, Xu L, Zhang Y, Lin X, Kong P, et al. Production of fibrinolytic enzyme from bacillus amyloliquefaciens by fermentation of chickpeas, with the evaluation of the anticoagulant and antioxidant properties of chickpeas. J Agric Food Chem. 2011;59(8):3957-63. doi:10.1021/jf1049535
12. Poernomo AT, Isnaeni, Purwanto. Thrombolytic Activity of Fibrinolytic Enzyme from Black Soybean Tempeh (Glycine Soja Sieb. Et Zucc) Fermented by Rhizopus Oligosporus FNCC 6010. Res J Pharm Biol Chem Sci. 2017;8(1):1885-96.
13. Sharma KM, Kumar R, Panwar S, Kumar A. Microbial alkaline proteases : Optimization of production parameters and their properties. J Genet Eng Biotechnol. 2017;15(1):115-26. doi:10.1016/j.jgeb.2017.02.001
14. Zhang S, Wang Y, Zhang N, Sun Z, Shi Y, Cao X, et al. Purification and characterisation of a fibrinolytic enzyme from Rhizopus micro sporus var. tuberosus. Food Technol Biotechnol. 2015;53(2):243-8. doi:10.17113/ftb.53.02.15.3874
15. Jennessen J, Schnürer J, Olsson J, Samson RA, Dijksterhuis J. Morphological characteristics of sporangiospores of the tempe fungus Rhizopus oligosporus differentiate it from other taxa of the R. microsporus group. Mycol Res. 2008;112(5):547-63. doi:10.1016/j.mycres.2007.11.006
16. Ahnan-winarno AD, Winarno FG, Gibbons J. Tempeh: A semicentennial review on its health benefits, fermentation, safety, processing, sustainability, and affordability. Compr Rev Food Sci Food Saf. 2021;20(2):1717-67. doi:10.1111/1541-4337.12710
17. Lim J, Nguyen TTH, Pal K, Kang CG, Park C, Kim SW, et al. Phytochemical properties and functional characteristics of wild turmeric (Curcuma aromatica) fermented with Rhizopus oligosporus. Food Chem X. 2021;13:100198. doi:10.1016/j.fochx.2021.100198
18. Nout MJR, Kiers JL. Tempe fermentation, innovation and functionality: update into the third millenium. J Appl Microbiol. 2005;98(4):789-805. doi:10.1111/j.1365-2672.2004.02471.x
19. Srivastava N, Srivastava M, Ramteke W, Mishra K. Chapter 23 - Solid-State Fermentation Strategy for Microbial Metabolites Production: An Overview. In: Gupta VK, Pandey A, editors. New and Future Developments in Microbial Biotechnology and Bioengineering: Microbial Secondary Metabolites Biochemistry and Applications. Amsterdam: Elsevier; 2019. p. 345-54. doi:10.1016/B978-0-444-63504-4.00023-2
20. Ahamed NA, Arif IA, Al-rashed S, Panneerselvam A, Ambikapathy V. In vitro thrombolytic potential of fibrinolytic enzyme from Brevibacterium sp. isolated from the root of the plant, Aloe castellorum. J King Saud Univ Sci. 2022;34(3):101868. doi:10.1016/j.jksus.2022.101868
21. Jo C, Zhang J, Tam JM, Church GM, Khalil AM, Segrè D, et al. Unlocking the magic in mycelium: Using synthetic biology to optimize filamentous fungi for biomanufacturing and sustainability. Mater Today Bio. 2023;19:100560. doi:10.1016/j.mtbio.2023.100560
22. Hermansyah B, Lokapirnasari WP. Pengaruh Subtitusi Tepung Biji Bunga Matahari (Helianthus Annuus L.) dalam Pakan Komersial dengan Konsentrasi Tertentu Terhadap Performa Ayam Pedaging. J Med Vet. 2019;2(1):7-12. doi:10.20473/jmv.vol2.iss1.2019.7-12
23. Lakshmi NJ, Vanaja M, Yadav SK, Maheswari M, Archana G, Patil A, et al. Effect of CO2 on growth, seed yield and nitrogen uptake in sunflower. J Agrometeorol. 2017;19(3):195-9. doi:10.54386/jam.v19i3.620
24. Franco R, Iseppi L, Taverna M. Sunflower Oil Functional Properties for Specialty Food. Nutr Food Sci Int J. 2018;5(4):4-7. doi:10.19080/nfsij.2018.05.555668
25. Karefyllakis D, van der Goot AJ, Nikiforidis CV. Multicomponent emulsifiers from sunflower seeds. Curr Opin Food Sci. 2019;29:35-41. doi:10.1016/j.cofs.2019.07.005
26. Grasso S, Pintado T, Pérez-Jiménez J, Ruiz-Capillas C, Herrero AM. Potential of a sunflower seed by-product as animal fat replacer in healthier frankfurters. Foods. 2020;9(4):445. doi:10.3390/foods9040445
27. Özacar M, Mehde AA, Mehdi WA, Özacar ZZ, Severgün O. The novel multi cross-linked enzyme aggregates of protease, lipase, and catalase production from the sunflower seeds, characterization and application. Colloids Surf B Biointerfaces. 2019;173:58-68. doi:10.1016/j.colsurfb.2018.09.042
28. Rauf A, Irfan M, Nadeem M, Ahmed I, Iqbal HMN. Optimization of Growth Conditions for Acidic Protease Production from Rhizopus oligosporus through Solid State Fermentation of Sunflower Meal. Int J Biotechnol Bioeng. 2010;4(12):898-901. doi:10.5281/zenodo.1079814
29. Celmeli T, Sari H. The Nutritional Content of Common Bean (Phaseolus vulgaris L.) Landraces in Comparison to Modern Varieties. Agronomy. 2018;8(9):166. doi:10.3390/agronomy8090166
30. Rodríguez L, Mendez D, Montecino H, Carrasco B, Arevalo B, Palomo I, et al. Role of Phaseolus vulgaris L. in the Prevention of Cardiovascular Diseases-Cardioprotective Potential of Bioactive Compounds. Plants. 2022;11(2):186. doi:10.3390/plants11020186
31. Chávez-Mendoza C, Hernández-Figueroa KI, Sánchez E. Antioxidant capacity and phytonutrient content in the seed coat and cotyledon of common beans (Phaseolus vulgaris L.) from various regions in Mexico. Antioxidants. 2019;8(1):5. doi:10.3390/antiox8010005
32. Poernomo AT, Isnaeni, Purwanto. Aktivitas Invitro Enzim Fibrinolitik Ekstrak Tempe Hasil Fermentasi Rhizopus Oligosporus ATCC 6010 Pada Substrat Kedelai Hitam. Berkala Ilmiah Kimia Farmasi. 2015;4(2):19-26.
33. Sambo S, Magashi AM, Farouq AA, Hassan SW. An overview of the solid state fermentation in the production of fungal protease enzymes. World J Adv Res Rev. 2021;9(3):85-9. doi:10.30574/wjarr.2021.9.3.0061
34. Susanti E, Lutfiana N, Suharti, Retnosari R. Screening of proteolytic bacteria from tauco Surabaya based on pathogenicity and selectivity of its protease on milky fish (Chanos chanos) scales for healthy and halal collagen production. IOP Conf Ser Mater Sci Eng. 2019;509:012044. doi:10.1088/1757-899X/509/1/012044
35. Muisristanto D, Poernomo AT, Sugijanto. Isolasi dan Penapisan Fibrinolitik Jamur Tanah Hutan Mangrove Wonorejo Surabaya. Berkala Ilmiah Kimia Farmasi. 2015;4(2):11-7.
36. Handoyo T, Morita N. Structural and Functional Properties of Fermented Soybean (Tempeh) by Using Rhizopus oligosporus. Int J Food Prop. 2006;9(2)347-55. doi:10.1080/10942910500224746
37. Upgade A, Nandeshwar A, Samant L. Assessment of fungal protease enzyme from French bean using A. niger by Solid State Fermentation. J Microbiol Biotechnol Res. 2011;1(4):45-51.
38. Raju EVN, Divakar G. An Overview on microbial fibrinolytic proteases. Int J Pharm Sci Res. 2014;5(3):643-56. doi:10.13040/IJPSR.0975-8232.5(3).643-56
39. Rashad MM, Mahmoud AE, Al-Kashef AS, Nooman MU. Purification and characterization of a novel fibrinolytic enzyme by Candida guilliermondii grown on sunflower oil cake. J Appl Sci Res. 2012;8(2):635-45.
40. Akhtar T, Hoq M, Mazid A. Bacterial Proteases as Thrombolytics and Fibrinolytics. Dhaka Univ J Pharm Sci. 2017;16(2):255-69. doi:10.3329/dujps.v16i2.35265
41. Gond SP, Sharma RA. Agro Waste Mediated Production of Fibrinolytic Enzyme and Its Optimization and Application. Int J Sci Res. 2022;11(2):58-63. doi:10.21275/SR22130105418
Authors
1.
Lusiana R, Poernomo AT, Syahrani A. Fibrinolytic Protease Activity of Crude Enzyme from Fermented Sunflower (Helianthus annuus) and Common Bean (Phaseolus vulgaris) seeds by Rhizopus microsporus var. oligosporus FNCC 6010 in Solid State Fermentation. Borneo J Pharm [Internet]. 2023Aug.30 [cited 2024Apr.29];6(3):295-304. Available from: https://journal.umpr.ac.id/index.php/bjop/article/view/4665
Copyright (c) 2023 Rebhika Lusiana, Achmad Toto Poernomo, Achmad Syahrani
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