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Bioactive Compounds from Microalgae Spirulina platensis as Antibacterial Candidates Against Pathogen Bacteria

1Research Center for Biotechnology, National Research and Innovation Agency, Jl Raya Bogor km 46, Cibinong, Bogor 16911, Indonesia

2Department of Pharmacy, Sekolah Tinggi Teknologi Industri dan Farmasi (STTIF), Bogor, Indonesia

Received: 6 Aug 2021; Revised: 31 Jan 2022; Accepted: 5 Feb 2022; Available online: 26 Feb 2022; Published: 28 Feb 2022.
Open Access Copyright 2022 Jurnal Kimia Sains dan Aplikasi under http://creativecommons.org/licenses/by-sa/4.0.

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Abstract

Microbial infection by bacteria has caused severe health problems worldwide. Treatment with antibiotics as the current solution has several drawbacks and triggers the phenomenon of bacterial resistance. Therefore, there is an urgency to look for a natural antimicrobial that is safer and has fewer side effects. One of the most promising antibacterial agents is Spirulina platensis. This research was conducted to evaluate the antibacterial activity of microalgae S. platensis against Propionibacterium acne, Staphylococcus epidermidis, and Enterobacter aerogenes and identify compounds from the active fraction of microalgae. Biomass was extracted with ethanol 96% using the reflux method then partitioned with immiscible solvents such as hexane, ethyl acetate, and water. Partial purification was carried out by chromatography techniques such as thin-layer chromatography and column chromatography. The compounds of active fractions were identified by GC-MS analysis. The result showed that ethyl acetate extract had vigorous antibacterial activity against all tested bacteria. The highest activity (14.4 ± 0.63 mm and 16.9 ± 1.48 mm) was achieved against P. acne; followed by S. epidermidis (13.05± 0.14 mm and 13.15 ± 0.0 mm), and E. aerogenes (11.7 ± 2.05 mm and 12.6 ± 1.90 mm), at concentrations 20,000 ppm and 30,000 ppm, respectively. The results indicated that the extract is more sensitive to Gram-positive bacteria (P. acne and S. epidermidis) than Gram-negative bacteria (E. aerogenes). Purification of the extract resulted in fraction 2 and fraction 6 as the most potential fractions for further analysis and identification. Based on the antibacterial activity, inhibition zones of fractions are wider than extracts. It could be assumed that the purification process enhances the activity of a sample. GC-MS analysis revealed that the dominant compounds of fractions 2 and 6 were bis (2-ethylhexyl) phthalate (67.76%) and 1,2-Benzendicarboxilic acid, bis (2-ethylhexyl) ester (50,88%), respectively. This result indicated that the ethyl acetate fraction of the microalgae S. platensis has the potential as a natural antibacterial.

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Keywords: Spirulina platensis; antibacterial; ethyl acetate fraction; purification; active compounds
Funding: National Research and Innovation Agency

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  1. Jyotirmayee Pradhan, Sachidananda Das, Basanta Kumar Das, Antibacterial activity of freshwater microalgae: A review, African Journal of Pharmacy and Pharmacology, 8, 32, (2014), 809-818 https://doi.org/10.5897/AJPP2013.0002
  2. Chikao Nishino, Nobuyasu Enoki, Shinkichi Tawata, Akihisa Mori, Koji Kobayashi, Masako Fukushima, Antibacterial activity of flavonoids against Staphylococcus epidermidis, a skin bacterium, Agricultural and Biological Chemistry, 51, 1, (1987), 139-143 https://doi.org/10.1080/00021369.1987.10867965
  3. Zartash Z. Khan, Maha A. Assi, Thomas A. Moore, Recurrent Epidural Abscess Caused by Propionibacterium Acnes, Kansas Journal of Medicin, 2, 4, (2009), 92-95 https://doi.org/10.17161/kjm.v2i4.11302
  4. Marco Nuno De Canha, Navneet Kishore, Vivek Kumar, Debra Meyer, Shamshun Nehar, B. Singh, Namrita Lall, The potential of Clausena anisata (Willd.) Hook. f. ex Benth against Propionibacterium acnes, South African Journal of Botany, 119, (2018), 410-419 https://doi.org/10.1016/j.sajb.2018.09.019
  5. Yuto Kamei, Miyuki Sueyoshi, Ken-ichiro Hayashi, Ryuta Terada, Hiroshi Nozaki, The novel anti-Propionibacterium acnes compound, Sargafuran, found in the marine brown alga Sargassum macrocarpum, The Journal of Antibiotics, 62, 5, (2009), 259-263 https://doi.org/10.1038/ja.2009.25
  6. Lu-Te Chuang, Tsung-Hsien Tsai, Tsung-Jung Lien, Wen-Cheng Huang, Jun-Jen Liu, Hsiang Chang, Mei-Ling Chang, Po-Jung Tsai, Ethanolic extract of Origanum vulgare suppresses Propionibacterium acnes-induced inflammatory responses in human monocyte and mouse ear edema models, Molecules, 23, 8, (2018), 1-11 https://doi.org/10.3390/molecules23081987
  7. Anne Davin-Regli, Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment, Frontiers in Microbiology, 6, 392, (2015), 1-10 https://doi.org/10.3389/fmicb.2015.00392
  8. Sunjukta Ahsan, Md Shamsul Arefin, John Litol Munshi, Mst Nadira Begum, Maisha Maliha, Sahida Rahman, Anindita Bhowmik, Md Shahidul Kabir, In vitro antibacterial activity of Spirulina platensis extracts against clinical isolates of Salmonella enterica serovars Typhi and Paratyphi (SUBP03), Stamford Journal of Microbiology, 5, 1, (2015), 22-25 https://doi.org/10.3329/sjm.v5i1.26916
  9. Shir Reen Chia, Kit Wayne Chew, Pau Loke Show, Ao Xia, Shih-Hsin Ho, Jun Wei Lim, Spirulina platensis based biorefinery for the production of value-added products for food and pharmaceutical applications, Bioresource Technology, 289, 121727, (2019), 1-8 https://doi.org/10.1016/j.biortech.2019.121727
  10. Vinay Kumar, A. K. Bhatnagar, J. N. Srivastava, Antibacterial activity of crude extracts of Spirulina platensis and its structural elucidation of bioactive compound, Journal of Medicinal Plants Research, 5, 32, (2011), 7043-7048 http://dx.doi.org/10.5897/JMPR11.1175
  11. Hooi Ren Lim, Kuan Shiong Khoo, Kit Wayne Chew, Chih-Kai Chang, Heli Siti Halimatul Munawaroh, P Senthil Kumar, Nguyen Duc Huy, Pau Loke Show, Perspective of Spirulina culture with wastewater into a sustainable circular bioeconomy, Environmental Pollution, 284, 117492, (2021), 1-13 https://doi.org/10.1016/j.envpol.2021.117492
  12. Touria Ould Bellahcen, Mounia Cherki, José Antonio Cayuela Sánchez, Abdelmjid Cherif, Abdelaziz El Amrani, Chemical Composition and Antibacterial Activity of the Essential Oil of Spirulina platensis from Morocco, Journal of Essential Oil Bearing Plants, 22, 5, (2019), 1265-1276 https://doi.org/10.1080/0972060X.2019.1669492
  13. Erismar Amri, Abdi Dharma, Armaini, Djong Hon Tjong, Screening anti-acne potency of microalgae: antibacterial and antioxidant activities, Der Pharma Chemica, 9, 4, (2017), 28-31
  14. G Usharani, G Srinivasan, S Sivasakthi, P Saranraj, Antimicrobial activity of Spirulina platensis solvent extracts against pathogenic bacteria and fungi, Advances in Biological Research, 9, 5, (2015), 292-298
  15. Véronique Seidel, Initial and bulk extraction, in: S.D. Sarker, Z. Latif, A.I. Gray (Eds.) Natural Products Isolation. Methods in Biotechnology, Humana Press, 2006, https://doi.org/10.1385/1-59259-955-9:27
  16. Hideaki Otsuka, Purification by solvent extraction using partition coefficient, in: Natural Products Isolation, Humana Press, 2006, https://doi.org/10.1385/1-59259-955-9:269
  17. Norman R. Farnsworth, Biological and phytochemical screening of plants, Journal of Pharmaceutical Sciences, 55, 3, (1966), 225-276 https://doi.org/10.1002/jps.2600550302
  18. J. B. Harborne, Methods of plant analysis, in: Phytochemical Methods, Springer, 1984, https://doi.org/10.1007/978-94-009-5570-7
  19. Simon Gibbons, An introduction to planar chromatography, in: S.D. Sarker (Ed.) Natural Products Isolation, Humana Press, 2006, https://doi.org/10.1385/1-59259-955-9:77
  20. Gino M Salituro, Claude Dufresne, Isolation by low-pressure column chromatography, in: Natural Products Isolation, Humana Press, 1998, https://doi.org/10.1007/978-1-59259-256-2_4
  21. Sheng-Yi Chiu, Chien-Ya Kao, Chiun-Hsun Chen, Tang-Ching Kuan, Seow-Chin Ong, Chih-Sheng Lin, Reduction of CO2 by a high-density culture of Chlorella sp. in a semicontinuous photobioreactor, Bioresource Technology, 99, 9, (2008), 3389-3396 https://doi.org/10.1016/j.biortech.2007.08.013
  22. Larissa T. Pereira, Cristiane R. Lisboa, Jorge A. V. Costa, Leonardo M. da Rosa, Lisiane F. de Carvalho, Evaluation of protein content and antimicrobial activity of biomass from Spirulina cultivated with residues from the brewing process, Journal of Chemical Technology & Biotechnology, 97, 1, (2022), 160-166 https://doi.org/10.1002/jctb.6925
  23. Joko Prayitno, Pola Pertumbuhan dan Pemanenan Biomassa dalam Fotobioreaktor Mikroalga untuk Penangkapan Karbon, Jurnal Teknologi Lingkungan, 17, 1, (2016), 45-52 https://doi.org/10.29122/jtl.v17i1.1464
  24. Avigad Vonshak, Spirulina platensis arthrospira: physiology, cell-biology and biotechnology, 1st ed., CRC press, London, 1997, https://doi.org/10.1201/9781482272970
  25. Gao-Xue Wang, Zhuang Zhou, Dong-Xin Jiang, Jing Han, Jian-Fu Wang, Liang-Wei Zhao, Jun Li, In vivo anthelmintic activity of five alkaloids from Macleaya microcarpa (Maxim) Fedde against Dactylogyrus intermedius in Carassius auratus, Veterinary Parasitology, 171, 3-4, (2010), 305-313 https://doi.org/10.1016/j.vetpar.2010.03.032
  26. Samad Tavakoli, Hui Hong, Kai Wang, Qingfeng Yang, Hadi Hashemi Gahruie, Shuai Zhuang, Yan Li, Yifan Liang, Yuqing Tan, Yongkang Luo, Ultrasonic-assisted food-grade solvent extraction of high-value added compounds from microalgae Spirulina platensis and evaluation of their antioxidant and antibacterial properties, Algal Research, 60, 102493, (2021), 1-10 https://doi.org/10.1016/j.algal.2021.102493
  27. Satyajit D. Sarker, Lutfun Nahar, Hyphenated Techniques, in: S.D. Sarker, Z. Latif, A.I. Gray (Eds.) Natural Products Isolation. Methods in Biotechnology, Humana Press, 2006, https://doi.org/10.1385/1-59259-955-9:233
  28. W. W. Davis, T. R. Stout, Disc plate method of microbiological antibiotic assay. I. Factors influencing variability and error, Applied and Environmental Microbiology Journal, 22, 4, (1971), 659-665 https://doi.org/10.1128/am.22.4.659-665.1971
  29. Marie B. Coyle, Manual of antimicrobial susceptibility testing, American Society for Microbiology, Washington, DC, 2005,
  30. M. Naviner, J-P Bergé, P. Durand, H. Le Bris, Antibacterial activity of the marine diatom Skeletonema costatum against aquacultural pathogens, Aquaculture, 174, 1-2, (1999), 15-24 https://doi.org/10.1016/S0044-8486(98)00513-4
  31. Michael T. Madigan, John M. Martinko, Jack Parker, Brock Biology of Microorganisms, 10th ed., Prentice Hall/Pearson Education, Upper Saddle River, NJ, 2003
  32. Jean Paul Dzoyem, Hiroshi Hamamoto, Barthelemy Ngameni, Bonaventure Tchaleu Ngadjui, Kazuhisa Sekimizu, Antimicrobial action mechanism of flavonoids from Dorstenia species, Drug Discoveries & Therapeutics, 7, 2, (2013), 66-72 https://doi.org/10.5582/ddt.2013.v7.2.66
  33. T. P. Tim Cushnie, Andrew J. Lamb, Antimicrobial activity of flavonoids, International Journal of Antimicrobial Agents, 26, 5, (2005), 343-356 https://doi.org/10.1016/j.ijantimicag.2005.09.002
  34. B. R. Min, W. E. Pinchak, R. Merkel, S. Walker, G. Tomita, R. C. Anderson, Comparative antimicrobial activity of tannin extracts from perennial plants on mastitis pathogens, Scientific Research and Essay, 3, 2, (2008), 066-073 https://doi.org/10.5897/SRE.9000280
  35. Keitarou Suzuki, Nahoko Nakano, Rie Tanaka, Masaru Uyeda, Motoo Shibata, Cell aggregation factor produced by Streptomyces sp. strain No. A-3315, Agricultural and Biological Chemistry, 52, 10, (1988), 2589-2595 https://doi.org/10.1080/00021369.1988.10869084
  36. B Uma, R Parvathavarthini, Antibacterial effect of hexane extract of sea urchin, Temnopleurus alexandri (Bell, 1884), International Journal of PharmTech Research, 2, 3, (2010), 1677-1680
  37. Pravat Manjari Mishra, A. Sree, Antibacterial activity and GCMS analysis of the extract of leaves of Finlaysonia obovata (a mangrove plant), Asian Journal of Plant Sciences, 6, 1, (2007), 168-172 https://dx.doi.org/10.3923/ajps.2007.168.172
  38. Anis Ben Hsouna, Mohamed Trigui, Riadh Ben Mansour, Raoudha Mezghani Jarraya, Mohamed Damak, Samir Jaoua, Chemical composition, cytotoxicity effect and antimicrobial activity of Ceratonia siliqua essential oil with preservative effects against Listeria inoculated in minced beef meat, International Journal of Food Microbiology, 148, 1, (2011), 66-72 https://doi.org/10.1016/j.ijfoodmicro.2011.04.028
  39. A. G. Jualang, M. Azlinah, P. C. Lee, S. E. How, Antibacterials and phytochemicals investigations of Chromolaenaodorata odorata (LF) King and Robinson (Asteraceae) from Sabah, Malaysia, Journal of Environmental Microbiology and Toxicology, 1, 1, (2013), 18-21 https://doi.org/10.54987/jemat.v1i1.31
  40. Miguel Herrero, Alejandro Cifuentes, Elena Ibañez, Sub-and supercritical fluid extraction of functional ingredients from different natural sources: Plants, food-by-products, algae and microalgae: A review, Food Chemistry, 98, 1, (2006), 136-148 https://doi.org/10.1016/j.foodchem.2005.05.058
  41. Irene Rodríguez-Meizoso, Laura Jaime, Susana Santoyo, Francisco J Señoráns, Alejandro Cifuentes, Elena Ibáñez, Subcritical water extraction and characterization of bioactive compounds from Haematococcus pluvialis microalga, Journal of Pharmaceutical and Biomedical Analysis, 51, 2, (2010), 456-463 https://doi.org/10.1016/j.jpba.2009.03.014
  42. Lamia Sakka Rouis-Soussi, Asma El Ayeb-Zakhama, Aouni Mahjoub, Guido Flamini, Hichem Ben Jannet, Fethia Harzallah-Skhiri, Chemical composition and antibacterial activity of essential oils from the Tunisian Allium nigrum L, EXCLI Journal, 13, (2014), 526 http://dx.doi.org/10.17877/DE290R-170
  43. Hatice Taner Saraçoğlu, Mehtap Akin, Betül Demirci, Kemal Hüsnü Can Başer, Chemical composition and antibacterial activity of essential oils from different parts of some Bupleurum L. species, African Journal of Microbiology Research, 6, 12, (2012), 2899-2908 https://doi.org/10.5897/AJMR11.1277
  44. Elija Khatiwora, Vaishali B. Adsul, Manik Kulkarni, N. R. Deshpande, R. V. Kashalkar, Antibacterial activity of Dibutyl Phthalate: A secondary metabolite isolated from Ipomoea carnea stem, Journal of Pharmacy Research, 5, 1, (2012), 150-152
  45. Syeda Farina Asghar, M. I. Choudahry, Gas chromatography-mass spectrometry (GC-MS) analysis of petroleum ether extract (oil) and bio-assays of crude extract of Iris germanica, International Journal of Genetics and Molecular Biology, 3, 7, (2011), 95-100 https://doi.org/10.5897/IJGMB.9000024
  46. Shujuan Chen, Jiajia Liu, Hanxiang Gong, Dongliang Yang, Identification and antibacterial activity of secondary metabolites from Taxus endophytic fungus, Sheng Wu Gong Cheng Xue Bao, 25, 3, (2009), 368-374
  47. Yousry M. Gohar, Manal M. A. El-Naggar, Magdy K. Soliman, Khouloud M. Barakat, Characterization of marine Burkholderia cepacia antibacterial agents, Journal of Natural Products, 3, (2010), 86-94
  48. Marjorie Murphy Cowan, Plant products as antimicrobial agents, Clinical Microbiology Reviews, 12, 4, (1999), 564-582 https://doi.org/10.1128/CMR.12.4.564
  49. A. T. K. Pratita, M. Fathurohman, R. Ruswanto, R. Suhartati, Potential of autotroph microalgae (spirulina plantentis) as antimicrobial agent, Journal of Physics: Conference Series, 2019 http://dx.doi.org/10.1088/1742-6596/1179/1/012173

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