Thrombolytic potential in bacteria isolated from fermented durian tempoyak

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CHRISTY PRISKILA
VALERIE VIDIAN
ASTIA SANJAYA
MARCELIA SUGATA
REINHARD PINONTOAN

Abstract

Abstract. Priskila C, Vidian V, Sanjaya A, Sugata M, Pinontoan R. 2022. Thrombolytic potential in bacteria isolated from fermented durian tempoyak. Biodiversitas 23: 5731-5737. Cardiovascular disease is one of the leading causes of death worldwide and is primarily caused by dysregulation in the blood clotting system leading to the formation of unwanted blood clots (thrombi). Thrombolytic therapy, which aims to break down unwanted blood clots, employs various agents possessing thrombolytic activity. However, the harmful side effects of conventional thrombolytic agents necessitate the exploration of new and safer agents with high thrombolytic activities. Thrombolytic agents can be obtained from various sources, including fermented foods. Tempoyak is a condiment made from fermented durian, which is found in some regions of Indonesia, and is reported to contain beneficial microorganisms. The aim of this study was to isolate and identify thrombolytic agents from tempoyak. After several pure microbial colonies were successfully isolated from tempoyak, they were screened for proteolytic activity on skim milk agar medium. The isolated colonies with proteolytic activity were then subjected to several tests, including the whole blood clot lysis test, euglobulin clot lysis test, fibrin plate method, and zymography. Subsequently, the isolates with thrombolytic and fibrinolytic activity potential were identified in terms of their morphology and biochemistry. In this study, three bacteria with thrombolytic activity potential were successfully isolated. Fibrin zymography indicated that the molecular weights of the proteins that play roles in the fibrinolytic activity ranged from approximately 30 to 153 kDa, which were suspected to correspond to serine protease, cysteine protease, and/or metalloprotease. All three isolates were identified as belonging to the genus Corynebacterium. This is the first report discussing the thrombolytic and fibrinolytic activities of Corynebacterium sp. derived from fermented food.

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References
Ali MR, Hossain MS, Islam MA, Arman MSI, Raju GS, Dasgupta P, Noshin TF. 2014. Aspect of thrombolytic therapy: a review. Sci World J 2014: 586510. DOI:10.1155/2014/586510.
Alibi S, Ferjani A, Boukadida J. 2016. Implication of Corynebacterium species in food’s contamination. J Coast Life Med 4: 416-419. DOI:10.12980/jclm.4.2016J6-26.
Alkarithi G, Duval C, Shi Y, Macrae FL, Ariëns RAS. 2021. Thrombus structural composition in cardiovascular disease. ATVB 41: 2370-2383. DOI:10.1161/ATVBAHA.120.315754.
Altaf F, Wu S, Kasim V. 2021. Role of fibrinolytic enzymes in anti-thrombosis therapy. Front Mol Biosci 8: 680397. DOI:10.3389/fmolb.2021.680397.
American Society for Microbiology. 2010. Catalase Test Protocol. https://asm.org/Protocols/Catalase-Test-Protocol.
American Society for Microbiology. 2012. Gelatin Hydrolysis Test Protocol. https://asm.org/ASM/media/Protocol-Images/Gelatin-Hydrolysis-Test-Protocol.pdf?ext=.pdf.
American Society for Microbiology. 2012. Starch Agar Protocol. https://asm.org/ASM/media/Protocol-Images/Starch-Agar-Protocol.pdf?ext=.pdf.
Aragosa A, Specchia V, Frigione M. 2020. PHB produced by bacteria present in the argan field soil: a new perspective for the synthesis of the bio-based polymer. Proc 69: 5. DOI:10.3390/CGPM2020-07226.
Bannish BE, Chernysh IN, Keener JP, Fogelson AL, Weisel JW. 2017. Molecular and physical mechanisms of fibrinolysis and thrombolysis from mathematical modeling and experiments. Sci Rep 7: 6914. DOI:10.1038/s41598-017-06383-w.
Bayot ML, Mirza TM, Sharma S. 2021. Acid Fast Bacteria. StatPearls, Treasure Island.
Burkovski A. 2015. Corynebacterium pseudodiphtheriticum: putative probiotic, opportunistic infector, emerging pathogen. Virulence 6: 673-674. DOI:10.1080/21505594.2015.1067747.
?epl JJ, Pátková I, Blah?šková A, Cvr?ková F, Markoš A. 2010. Patterning of mutually interacting bacterial bodies: close contacts and airborne signals. BMC Microbiol 10: 139. DOI:10.1186/1471-2180-10-139.
Daas MS, Acedo JZ, Rosana ARR, Orata FD, Reiz B, Zheng J, Nateche F, Vederas JC. 2018. Bacillus amyloliquefaciens spp. plantarum F11 isolated from Algerian salty lake as a source of biosurfactants and bioactive lipopeptides. FEMS Microbiol Lett 365: 248-250. DOI:10.1093/femsle/fnx248.
Dikson, Victor H, Jong D, Sanjaya A, Samantha A, Jo J, Pinontoan R. 2022. Whole-genome analysis of Bacillus subtilis G8 isolated from natto. Biodiv. 23: 1293-1300. DOI:10.13057/biodiv/d230313.
Farnia P, Farnia P, Ghanavi J, Zhavnerko GK, Poleschuyk NN, Velayati AA. 2018. A review on the shape changes in pathogenic bacteria with emphasis on Mycobacterium tuberculosis. BBRJ 2: 242-246. DOI:10.4103/bbrj.bbrj_86_18.
Garcia-Rivera G, Rodriguez MA, Ocadiz R, Martinez-Lopez MC, Arroyo R, Gonzalez-Robles A, Orozco E. 1999. Entamoeba histolytica?: a novel cysteine protease and an adhesin form the 112 kDa surface protein. Mol Microbiol 33: 556-568. DOI:10.1046/j.1365-2958.1999.01500.x.
Gladysheva I, Chertkov KL, Cherkasov SV, Khlopko YA, Kataev VY, Valyshev AV. 2021. Probiotic potential, safety properties, and antifungal activities of Corynebacterium amycolatum ICIS 9 and Corynebacterium amycolatum ICIS 53 strains. Probiotics Antimicrob Proteins, 2021. DOI:10.1007/s12602-021-09876-3.
Gunkova PI, Buchilina AS, Maksimiuk NN, Bazarnova YG, Girel KS. 2021. Carbohydrate fermentation test of lactic acid starter cultures. IOP Conf Ser Earth Environ Sci 852: 012035. DOI:10.1088/1755-1315/852/1/012035.
Hasanuddin. 2010. Mikroflora pada tempoyak. Agritech 30: 218-222. DOI:10.22146/agritech.9711. (In Bahasa Indonesia)
Hikmawati F, Susilowati A, Setraningsih R. 2019. Colony morphology and molecular identification of Vibrio spp.on green mussels (Perna viridis) in Yogyakarta, Indonesia tourism beach areas. Biodivers 20: 2891-2899. DOI:10.13057/biodiv/d201015.
Kotb, E. 2012. Fibrinolytic Bacterial Enzymes with Thrombolytic Activity. Springer, Berlin.
Janoir C, Pechine S, Grosdidier C, Collignon A. 2007. Cwp84, a surface-associated protein of Clostridium difficile, is a cysteine protease with degrading activity on extracellular matrix proteins. J Bacteriol 189: 7174-7180. DOI:10.1128/JB.00578-07.
Juliyarsi I, Hartini P, Yuherman, Djamaan A, Arief, Purwanto H, Aritonang SN, Hellyward J, Purwati E. 2018. Characterization of lactic acid bacteria and determination of antimicrobial activity in tempoyak from Padang Pariaman District, West Sumatra, Indonesia. Pak J Nutr 17: 506-511. DOI:10.3923/pjn.2018.506.511.
Lee MJ, Kim P. 2018. Recombinant protein expression system in Corynebacterium glutamicum and its application. Front Microbiol 9: 1-14. DOI:10.3389/fmicb.2018.02523.
Liang T-W, Lin J-J, Yen Y-H, Wang C-L, Wang S-L. 2006. Purification and characterization of a protease extracellularly produced by Monascus purpureus CCRC31499 in a shrimp and crab shell powder medium. Enzyme Microb Technol 38: 74-80. DOI:10.1016/j.enzmictec.2005.04.023.
Libretti S, Puckett Y. 2021. Physiology, Homeostasis. StatPearls Publishing, Treasure Island.
Lin C-Y, Wang J-K, Torri J, Dou L, Sang QA, Dickson RB. 1997. Characterization of a novel, membrane-bound, 80-kDa matrix-degrading protease from human breast cancer cells monoclonal antibody production, isolation, and localization. J Biol Chem 272: 9147-9152.
Lucy J, Raharjo PF, Elvina, Florencia L, Susanti AI, Pinontoan R. 2019. Clot lysis activity of Bacillus subtilis G8 isolated from Japanese fermented natto soybeans. Appl Food Biotechnol 6: 101-109. DOI:10.22037/afb.v6i2.22479.
Mackman N, Bergmeier W, Stouffer GA, Weitz JI. 2020. Therapeutic strategies for thrombosis: new targets and approaches. Nat Rev Drug Discov 19: 333-352. DOI:10.1038/s41573-020-0061-0.
Mahmoud A, Kotb E, Alqosaibi AI, Al-Karmalawy AA, Al-Dhuayan IS, & Alabkari H. 2021. In vitro and in silico characterization of alkaline serine protease from Bacillus subtilis D9 recovered from Saudi Arabia. Heliyon 7: e08148. DOI:10.1016/j.heliyon.2021.e08148.
Menberu MA, Liu S, Cooksley C, Hayes AJ, Psaltis AJ, Wormald P-J, Vreugde S. 2021. Corynebacterium accolens has antimicrobial activity against Staphylococcus aureus and methicillin-resistant S. aureus pathogens isolated from the sinonasal niche of chronic rhinosinusitis patients. Pathogens 10: 207. DOI:10.3390/pathogens10020207.
Menberu MA, Cooksley C, Ramezanpour M, Bouras G, Wormal P-J, Psaltis AJ, Vreugde S. 2022. In vitro and in vivo evaluation of probiotic properties of Corynebacterium accolens isolated from the human nasal cavity. Microbiol Res 255: 126927. DOI:10.1016/j.micres.2021.126927.
Mine Y, Wong AHK, Jiang B. 2005. Fibrinolytic enzymes in Asian traditional fermented foods. Food Res Int 38: 243-250. DOI:10.1016/j.foodres.2004.04.008.
Mogrovejo-Arias DC, Brill FHH, Wagner D. 2020. Potentially pathogenic bacteria isolated from diverse habitats in Spitsbergen, Svalbard. Environ Earth Sci, 79: 109. DOI:10.1007/s12665-020-8853-4.
Narzary Y, Das S, Goyal AK, Lam SS, Sarma H, Sharma D. 2021. Fermented fish products in South and Southeast Asian cuisine: indigenous technology processes, nutrient composition, and cultural signifcance. J Ethn Foods 8: 1-9. DOI:10.1186/s42779-021-00109-0.
Ouertani A, Chaabouni I, Mosbah A, Long J, Barakat M, Mansuelle P, Mghirbi O, Najjari A, Ouzari H-I, Masmoudi AS, Maresca M, Ortet P, Gigmes D, Mabrouk K, Cherif A. 2018. Two new secreted proteases generate a casein-derived antimicrobial peptide in Bacillus cereus foodborne isolate leading to bacterial competition in milk. Front Microbiol, 9: 1148. DOI:10.3389/fmicb.2018.01148.
Palta S, Saroa R, & Palta A. 2014. Overview of the coagulation system. Indian J Anaesth 58: 515-523. DOI:10.4103/0019-5049.144643.
Permana L, Pangastuti HA, Wahyuningtyas A. 2021. Young adult perception of fermented durian (tempoyak) in Lampung Province Indonesia. JSAT 5: 38-42. DOI:10.35472/jsat.v5i1.392.
Pinontoan R, Elvina, Sanjaya A, Jo J. 2021. Fibrinolytic characteristics of Bacillus subtilis G8 isolated from natto. BMFH 40: 144-149. DOI:10.12938/bmfh.2020-071.
Rojas-García LL. 2022. Coryneform gram-positive bacilli. In: Rezaei N (ed) Encyclopedia of Infection and Immunity. Elsevier, Amsterdam.
Romulo A, Surya R. 2021. Tempe: A traditional fermented food of Indonesia and its health benefits. Int J Gastron Food Sci 26: 100413. DOI:10.1016/j.ijgfs.2021.100413.
Rosendaal FR. 2016. Causes of venous thrombosis. Thromb J 14: 117-121. DOI:10.1186/s12959-016-0108-y.
Saimin J, Hartati, Purnamasari Y, Mulyawati SA, Tien, Aritrina P. 2020. Microbiological and biochemical contamination analysis of refilled drinking-water in Abeli, Kendari, Southeast Sulawesi. InaBJ 12: 124-129. DOI:10.18585/inabj.v12i2.871.
Salarizadeh N, Hasania S, Noghabi KA, Sajedi RH. 2014. Purification and characterization of 50 kDa extracellular metalloprotease from Serratia sp. ZF03. Iran J Biotechnol 12: 18-27. DOI:10.15171/IJB.1009.
Sgobba E, Blöbaum L, Wendisch VF. 2018. Production of food and feed additives from non-food-competing feedstocks: valorizing n-acetylmuramic acid for amino acid and carotenoid fermentation with Corynebacterium glutamicum. Front Microbiol 9: 1-11. DOI:10.3389/fmicb.2018.02046.
Shoaib M, Muzammil I, Hammad M, Bhutta ZA, Yaseen I. 2020. A mini-review on commonly used biochemical tests for identification of bacteria. Int J Sci Res Publ 54. DOI:10.47119/IJRP100541620201224.
Surono IS. 2016. Ethnic fermented foods and beverages of Indonesia. In Tamang JP (ed) Ethnic Fermented Foods and Alcoholic Beverages of Asia. Springer, Berlin.
Tamang JP, Watanabe K, Holzapfel WH. 2016. Review: diversity of microorganisms in global fermented foods and beverages. Front Microbiol, 7: 1-28. DOI:10.3389/fmicb.2016.00377.
Tripathi N, Sapra A. 2021. Gram Staining. StatPearls, Treasure Island.
Yoshioka M, Nakayama Y, Yoshida M, Ohashi K, Morita N, Kobayashi H, Yamamoto Y. 2010. Quality control of photosystem II: FtsH hexamers are localized near photosystem ii at grana for the swift repair of damage. J Biol Chem 285: 41972-41981. DOI:10.1074/jbc.M110.117432.
Yuliana N. 2012. Pengolahan durian (Durio zibethinus) fermentasi (tempoyak). JTIHP 12: 74-80. DOI:10.23960/jtihp.v12i2.74%20-%2080.
Zhang J, Ma G, Lu Z, Zhou Y, Wen C, Wu Y, Xu R. 2014. Targeted thrombolysis strategies for neuroprotective effect. Neural Regen Res 9: 1316-1322. DOI:10.4103/1673-5374.137580.
Zhang Z, Yuan Y, Ali MW, Peng T, Peng W, Raza MF, Zhao Y, Zhang H. 2018. Cultivable anaerobic and aerobic bacterial communities in the fermentation chambers of Holotrichia parallela (coleoptera:scarabaeidae) larvae. PLoS ONE 13: e0190663. DOI:10.1371/journal.pone.0190663.

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