Comparison of Antioxidant effects of Polysaccharides of Mixed Microalgae Isolates Glagah Beach Yogyakarta and East Java, Indonesia
Zhaza Afililla1, Mahendra Pujiyanto1, Lucia Tri Suwanti2,3*, Mochamad Donny Koerniawan4, Eko Agus Suyono5, Arief Budiman6, Ulfah Juniarti Siregar7, Heni Puspitasari3,
1Magister Student, Faculty of Veterinary Medicine, Universitas Airlangga.
Jl. Mulyorejo, Kampus C Unair, Surabaya 60115, East Java, Indonesia.
2Department of Veterinary Parasitology, Faculty of Veterinary Medicine,
Universitas Airlangga. Jl. Mulyorejo, Kampus C Unair, Surabaya 60115, East Java, Indonesia.
3Institute of Tropical Disease, Universitas Airlangga. Jl. Mulyorejo,
Kampus C Unair, Surabaya 60115, East Java, Indonesia.
4Department of Architecture, School of Architecture, Planning, and Policy Development,
Institut Teknologi Bandung. Jl. Ganesha No. 10, Bandung 40132, West Java, Indonesia.
5Department of Tropical Biology, Faculty of Biology, Universitas Gadjah Mada,
Jl. Teknika Selatan, Sleman 55281, Yogyakarta, Indonesia.
6Department of Chemical Engineering, Faculty of Engineering,
Universitas Gadjah Mada, Jl. Grafika 2, Sleman 55281, Yogyakarta, Indonesia.
7Department of Silviculture, Faculty of Forestry, Institut Pertanian Bogor.
Jl. Lingkar Akademik, Dramaga, Bogor 16680, West Java, Indonesia.
*Corresponding Author E-mail: lucia-t-s@fkh.unair.ac.id
ABSTRACT:
Indonesia is a country with a large marine and has a very high biodiversity of microalgae. Previous research has identified mixed microalgae from Glagah Beach, Yogyakarta, and several beaches in East Java. This study aims to extract polysaccharides and assessed the antioxidant activity of polysaccharides from those microalgae. Polysaccharides of Spirulina platensis, a mixed microalgae Glagah, and a mixed microalgae East Java were extracted by the alkaline method. The extraction rate and protein and carbohydrate content of polysaccharides of each of microalgae were calculated. The antioxidant activity of polysaccharides was observed in vitro using the DPPH assay method. The highest extraction rate was obtained from Glagah microalgae followed by S. platensis and East Java microalgae with values of 13.575%, 9.75%, and 2.375%, respectively. On the other hand, the carbohydrate content of the polysaccharides from Glagah microalgae was the lowest, followed by S. platensis and East Java microalgae, 1.2 mg/mL, 13.33 mg/mL, and 21.925 mg/mL, respectively. The protein content in polysaccharides from Glagah microalgae was the highest, followed by East Java microalgae and S. platensis the lowest, 2.23 mg/mL, 1.01 mg/mL, and 0.67 mg/mL, respectively. Based on the results of IC50 values, the antioxidant activity of mixed microalgae polysaccharides from Glagah and East Java was included in the active/moderate category, 125.21 µg/mL and 127.11 µg/mL, respectively, while the antioxidant activity of polysaccharide S. platensis was low, 171.82 µg/mL. In conclusion, Glagah and East Java Microalgae Polysaccharides have the opportunity to be promoted as health ingredients to overcome free radicals.
KEYWORDS: Antioxidant activity, Biodiversity, Marine, Microalgae, Polysaccharides.
INTRODUCTION:
Indonesia is a country with an aquatic environment that has a very high biodiversity of microalgae. Microalgae are eukaryotic photosynthetic microorganisms that utilize carbon dioxide and sunlight to form biomass1. It found in almost all habitats, both normal and extreme waters such as fresh water, lakes, rivers, oceans, estuaries, brackish, thermophilic, saline, and hyper-saline environments2,3, including in Indonesian marine waters. Recent research has discovered and developed mixed microalgae isolated from Glagah Beach Yogyakarta, which was later named the Glagah Consortium. The Glagah Consortium consists of 6 species of microalgae and 6 species of bacteria4. The six species of microalgae are Cyclotella polymorpha, Cylindrospermopsis raciborskii, Golenkinia radiata, Corethron criophilum, Chlamydomonas sp., and Syracosphaera turquoise, while the 6 species of bacteria are Corynebacterium ulcerans, Corynebacterium bovis, Bacillus cereus, Bacillus megaterium, Pediococcus parvulus, and Staphylococcus vitulinus4,5 Meanwhile, Zakiyah et al. found and identified 36 genera of mixed microalgae from East Java, Indonesia6.
Microalgae have been exploited as a potential biomass for raw materials in the health sector, cosmetics, aquaculture, and even for alternative fuels substitute for fossil fuels7. Important components contained in microalgae include hydrogen, lipids, hydrocarbons, carbohydrates, polysaccharides, vitamins, proteins, as well as various bioactive components such as antioxidants, anti-inflammatory, immunostimulant8,9 The bioactive components of microalgae include carotenoids, terpenoids, xanthophylls, chlorophyll, and alkaloids10. The total protein content of microalgae is range from 43 to 50% and its quality of is known to be similar to several sources of animal protein such as milk, meat and eggs11.
The antioxidant activity of microalgae is played by the polysaccharide component. Based on the place, polysaccharides from microalgae can be divided into two, intracellular and structural polysaccharides12. Structural polysaccharides include exopolysaccharides released in the medium, cell-bound polysaccharides, and cell wall polysaccharides13.
In recent years, several studies have proven that polysaccharides from natural products have a broad therapeutic effect and are beneficial for health. Polysaccharides are reported to have effective free radical and antioxidant activities and these activities have an important role in preventing damage to organizsms due to oxidative stress14. Zhang et al. stated that polysaccharides contained in five algae (including brown algae) have antioxidant activities15, as well as Wang et al., reported that polysaccharides extracted from red algae Gracilariopsis lemaneiformis had strong antioxidant activity16. In addition to antioxidants, other potential roles of microalgae in the medical and health world are as hepatoprotective, antihypersensitive, anticarcinogenic, anticoagulant, and immunomodulatory17.
Marine microalgae have been extensively researched, cultivated and exploited as an alternative to land plant commodities as a source of oil for biofuel production because of their ability to produce high biomass and can grow in a short time. Even though Indonesia has a high diversity of microalgae, its potential has not been fully utilized. Until now, the mixture of microalgae isolates from Glagah Yogyakarta has only been studied on the lipid profile as biodiesel material4, as well as isolates from East Java that have been identified as directed for biodiesel6. Khan et al. mentioned that the content of microalgae is varies9, polysaccharide is one of them and according to Balakrishnan et al., marine polysaccharides have been demonstrated to have antioxidant activity18. Antioxidants have become compounds of scientific interest because of their many health benefits including anti-aging and anti-inflammatory properties19. But, only a few genera of microalgae are commercialized as a source of antioxidants, for example Chlorella, Dunaliella, Spirulina, Nostoc, and Haemotococcus20. Therefore, this study was conducted to evaluate the antioxidant activity of polysaccharides of mixed microalgae Glagah and East Java compared to polysaccharides of Spirulina platensis, based on its free radical scavenging properties and IC50 value. This paper also describes the comparison of the extraction rate, protein and carbohydrate content of the three microalgae polysaccharides.
Materials and Methods:
Microalgae biomass and extraction:
The microalgae used were S. platensis
and microalgae Glagah Yogjakarta originally from the Faculty of Biology, Gadjah
Mada University, Yogyakarta, and mixed microalgae East Java was obtained from
the Faculty of Forestry, IPB University, Bogor. Polysaccharides were extracted
with the Lye Extraction Method21. Forty grams of microalgae powder was
added to 1.6 L of water in alkaline condition by added 1 mol/L NaOH until
the pH10. The solution was homogenized with a stirrer and incubated in an 80°C
water bath for 8 hours, followed by centrifugation with speed
4300 rpm, for 20 minutes. The supernatant was concentrated until
1/5 of its original volume. Five times the volume of 95% ethanol was added to
the concentrated solution and placed in the freezer overnight and followed by
centrifugation with speed 4300rpm, for 10 minutes. The precipitate was washed
by adding absolute acetone and then homogenized by vortex. The solution was
filtered and then freeze-dried for 2hours.
The extraction rate of polysaccharides was calculated by formula. Extraction rate = extracted polysaccharides/dry weight of microalgae powder × 100%. Protein content was determined by the Bradford Method. 10 µL of sample was added with 200 µL of Bradford's solution and 790µL of distilled water. As a blank solution: 200 µL of Bradford's solution was added with 790µL of distilled water. The absorbances were read at wavelength 595nm by a UV-Vis spectrophotometer. Protein concentration expressed in mg/ml. Meanwhile, the Phenol Sulfuric Acid assay was used for carbohydrate content determination. The sample solution (10µL) was diluted with distilled water (90µL). Then 50µL of 5% phenol was added. and homogenized by vortex for 1 minute. The solution was added with 2 mL of sulfuric acid and incubated for 10 minutes at room temperature. The blank solution was made from 50 µL of 5% phenol and 100µL of distilled water. Then, the absorbance was measured at a wave length 490nm.
Antioxidant activity test:
The antioxidant activity of microalgae polysaccharides was tested with free radical scavenging activity using DPPH (1,1-diphenyl-2-picrylhydrazyl)22. Solutions of each polysaccharide extract were prepared at graded concentrations (10, 12.5, 15, 25, 50, 75, 100, 125, 150 and 200µg/mL). Each sample was carried out in two replications for each concentration. Each 1 mL sample was mixed with 1mL of 30mmol/L DPPH-ethanol solutions, then then homogenized with a vortexed. The mixture was allowed to react for 30minutes at room temperature, and the absorbance was measured at 517 nm using a spectrophotometer. Free radical scavenging activity was calculated using the formula: DPPH scavenging effect (%) = [(AB - AA)/ AB] x 100. Where, AB = absorbance of DPPH solution (t = 0 min); AA = absorbance of tested extract solution (t = 30 min). Then plotted the percentage (%) inhibition against concentration and illustrated by the graph. IC50 was calculated by probit analysis.
RESULT AND DISCUSSION:
Extraction rate, carbohydrate content, and protein content of microalgae polysaccharides:
Extraction rate, carbohydrate content, and protein content of microalgae polysaccharides of Spirulina platensis, mixed microalgae Glagah, and mixed microalgae East Java were presented in Table 1. The highest extraction rate was obtained from Glagah microalgae followed by S. platensis and East Java microalgae with values of 13.575%, 9.75%, and 2.375% respectively. On the other hand, the carbohydrate content of the polysaccharides from Glagah microalgae was the lowest, followed by S. platensis and East Java microalgae, 1.2mg/mL, 13.33mg/mL, and 21.925 mg/mL, respectively. The protein content in polysaccharides from Glagah microalgae was the highest, followed by East Java microalgae and S. platensis the lowest, 2.23mg/mL, 1.01mg/mL, and 0.67 mg/mL, respectively.
Tabel 1: Extraction rate, carbohydrate content, and protein content of microalgae polysaccharides of Spirulina platensis, mixed microalgae Glagah, and mixed microalgae East Java
Microalgae |
Extraction rate (%) |
Carbohydrate content (mg/mL) |
Protein content (mg/mL) |
Spirulina platensis |
9.75 |
13.33 |
0.67 |
Mixed Microalgae Glagah |
13.575 |
1.2 |
2.23 |
Mixed Microalgae East Java |
2.375 |
21.925 |
1.01 |
DPPH radical scavenging activity:
Figure 1 shows the free radical scavenging activity of polysaccharides of microalgae. Among the extractives, Glagah Isolat possessed the highest activity. At a concentration of 200μg/mL, the scavenging activity of Spirulina, Glagah, and East Java Isolat was 51.57%, 55.65%, and 55.15%, respectively. The IC50 of of polysaccharides of Spirulina, Glagah, and East Java Isolat were 171.28µg/mL, 125.21µg/mL, and 127.11 µg/mL, respectively (Table 2).
Figure 1: In vitro antioxidant activity of microalgae polysaccharides. Y axis: DPPH radical scavenging activity (%), X axis: concentration (µg/mL)
Table 2: IC50 values of microalgae polysaccharides of Spirulina platensis, mixed microalgae Glagah, and mixed microalgae East Java
Microalgae |
IC50 values (µg/mL) |
Spirulina platensis |
171.82 |
Mixed Microalgae Glagah |
125.21 |
Mixed Microalgae East Java |
127.11 |
DISCUSSION:
Extraction rate, carbohydrate content, and protein content of microalgae polysaccharides
The synthesis and production of polysaccharides is a complex process, for that the extraction and purification of polysaccharides must be carried out aiming to achieve high yields, without other compounds12. The Lye Extraction method was chosen because this method is the most optimal compared to the other three methods, namely: Hot-Water Extraction, Ultrasound-Assisted Extraction, and Freeze -Tawing Method21. Similar results were presented by Afililla et al. who compared this method with the hot water method in terms of extraction rate, protein, and carbohydrate content23. The extraction rate of S. platensis in this study was higher than the results of Wang et al. research both with the same extraction method (Lye Extraction Method) and with different extraction methods (Hot-Water Extraction, Ultrasound-Assisted Extraction, and Freeze -Tawing Method)21.
The value of extraction rate and protein content of Glagah microalgae polysaccharides is the highest compared to the other two microalgae, presumably because Glagah microalgae is a mixed microalgae consisting of 6 species of bacteria and 6 species of microalgae4. According to Zeidan et al., bacteria are capable of producing a wide variety of polysaccharides with diverse biological functions, because bacteria can synthesize cytoplasmic storage polysaccharides (such as glycogen, bacterial starch) and cell surface-related polysaccharides (peptidoglycan, lipopolysaccharide, lipooligosaccharide, teichoic acid, lipoteichoic acid and other cell wall polysaccharides)24. The presence of bacteria in the Glagah microalgae turned out to be mutually beneficial. It is known that microalgae are often associated with a variety of specific bacteria in the environment of origin and culture sites25. Microalgae exhibit vigorous growth in the presence of a diverse bacterial community in culture. It is known that microalgae associate with microbiota in their phycosphere biofilms26. In addition, microalgae provide organic and inorganic compounds for bacterial growth27. Microbial species also affect the protein content. According to Villarruel-López et al. that the total protein content of biomass depends on the microbial species28. This difference may also be due to the origin of microalgae, because according to Wang et al., differences in cultivars, origins, and batches have been shown to have a significant influence on the physicochemical and structural properties of polysaccharides29. Morais et al. and Costa et al. also confirmed that the composition of microalgae polysaccharides depends on several factors, such as species, strains, and cultivation conditions (nutrient availability, salinity, irradiation, and temperature). This is also a possible reason why the carbohydrate content of the Glagah microalgae polysaccharides was lower than other polysaccharides in this study12,30. According to Moriera et al., microalgae carbohydrates consist mostly of galactose, xylose, and glucose, but other sugars may also be present, as well as residues of glucuronic and galacturonic acid31.
DPPH radical scavenging activity:
Polysaccharides are essential biomacromolecules, which are formed from several monosaccharides linked by glycosidic bonds. Polysaccharides derived from natural products are of great interest in antioxidant activity. Many studies have revealed that polysaccharides derived from marine organisms exhibit antioxidant activity, microalgae polysaccharides32. Many different in vitro models have been introduced to evaluate antioxidant activity to assess which antioxidants will be useful for food and biological systems29. In their review, Zong et al. described the method used to prove the antioxidant activity of marine organisms free radical scavenging activity using 2,2-diphenyl-1-picrylhydrazyl (DPPH), 2,2’-Azobis(2-amidinopropane) dihydrochloride (AAPH); 2,2’-Azino-bis (3-ethylbenzothiazoline-6-sulfonic acid (ABTS), hydroxyl radicals, peroxyl radicals, alkyl radicals, H2O2, superoxide radicals scavenging activities. In this study also used DPPH method, IC50 was used to determine the antioxidant capacity of the sample compared to the standard. IC50 DPPH scavenging capacity is the concentration of a sample that can inhibit 50% of the scavenging capacity of DPPH32. DPPH radical scavenging assay is among the most frequently used methods and offers the first approach for evaluating antioxidant activity, this method is a simple and does not require special sample treatment33. Its was common test for the spectrophotometric measurement of the total antioxidant activity in natural products34.
Antioxidant play an important role in food preservation by inhibiting oxidation processes and contributing to health promotion rendered by many dietary supplements, nutraceuticals and functional food ingredients33. Researchers classify antioxidant activity based on the IC50 value and the classification is slightly different for each researcher. According to Sukweenadi et al., a compound is classified as very strong when the IC50 value is <50ppm, strong when the IC50 value is 50-100ppm, moderate when the IC50 value is 101-150ppm, and weak antioxidants when the IC50 value is >150 ppm35. Fidrianny et al. classified antioxidant activity into 4 criteria, namely, IC50 < 50µg/mL is a very strong antioxidant, 50-100µg/mL is a strong antioxidant, 101-150µg/mL is a moderate antioxidant, while the antioxidant is weak with IC50 > 150µg/mL36. But, according to Lung and Destiani, the antioxidant intensity IC50 values are classified into 5 criteria. IC50 values less than 50 µg/ml is a very strong antioxidant, 50-100µg/ml is a strong antioxidant, 100-250µg/mL is a moderate antioxidant, 250-500µg/ml is a weak antioxidant, and IC50 more than 500µg/ml has no antioxidant activity37. Based on those criteria, the antioxidant activity of microalgae polysaccharides from Glagah and East Java isolates was moderate, while the antioxidant activity of Spirulina polysaccharides was weak. So, the antioxidant activity of mixed microalgae polysaccharides from Glagah and East Java was included in the active/moderate category, while the antioxidant activity of polysaccharide S. platensis was low37. The low antioxidant activity of Spirulina polysaccharides in this study is the same as the results of Margiati et al. who reported that the IC50 of Spirulina pycocyanin was more than 300µg/mL (311.43µg/mL and 387.36µg/mL)38. But the results of this study are lower than those of Zaid et al. that the antioxidant activity of Spirulina platensis water extracts is very high, namely 81.1% at a concentration of 200µg/mL39. The reason for the difference in antioxidant activity of spirulina is probably due to the source and method of extraction. The source of Spirulina platensis used by Zaid et al. was in the form of food supplement tablets were obtained from a company, while the source of Spirulina in this study was the result of cultures conducted by researchers from Gadjah Mada University Yogyakarta Indonesia39.
Zong et al. in their review summarized the activity of antioxidant polysaccharides derived from marine organisms reported during 2013–2019, including brown algae, red algae, green algae, microalgae, marine fungi, marine bacteria and marine animals. The antioxidant activity based on the IC50 value varies widely, depending on the origin of the polysaccharides and the method used. The difference in antioxidant activity is probably due to differences in the density of the polysaccharides being compared. The IC50 value which reflects the antioxidant activity in this study is related to the protein content of each microalga. The protein content of spirulina is the lowest (0.67mg/mL) so its antioxidant activity is the weakest. On the other hand, the protein content of mixed microalgae Glagah is the highest (2.23mg/mL) thus it has the strongest antioxidant activity32. Microalga polysaccharides are described as being mainly heteropolysaccharides generally related to other components12. According to Wang et al. natural polysaccharides do not always exist singly but are conjugated with other components, such as amino acids, proteins, lipids, and nucleic acid residues, and sometimes polysaccharide conjugates act as antioxidants and the content of protein in polysaccharide extracts appeared to contribute a direct scavenging effect29. Another researcher stated that proteins or peptides may also act as polysaccharide conjugates to enhance the antioxidant activity of polysaccharides40,41. Nemzer et al. also reported that the antioxidant activity contained in tea polysaccharides depends on the protein and polyphenol content14. Various types of extracts showed that carotenoid and phenolic compounds contributed significantly to the antioxidant capacity of microalgae42. The the antioxidant activity of microalgal polysaccharides was also related to the presence of phenols and flavonoids43,44.
Based on the high rate of extraction, protein polysaccharide content and antioxidant activity, the Glagah microalgae polysaccharide can be developed as a functional food. This is in line with the statement of Chia et al., that the quality of microalgae protein is known to be similar to several sources of animal protein such as milk, meat and eggs11. Moreira et al. also stated that microalgae polysaccharides hold promise as a potential alternative in several sectors, including the food, animal feed, and agriculture sectors31. Luo et al. found that Spirulina platensis polysaccharide had strong antioxidant activity and used it for sauce preservatives45. The microalgae polysaccharide can condense into a film on the surface of the food, reducing the damage to the surface of the food, minimizing and inhibiting the metabolism of fruits and vegetables and water evaporation, and extending the shelf life of fruits and vegetables46,47,48. Our previous research has shown that microalgae polysaccharides from Glagah Beach, Jogyakarta and several beaches in East Java have potential as immunomodulators and as anti-malarials in vitro23,47.
Conclusion:
Polysaccharides of Mixed Microalgae from Glagah Yogyakarta and East Java Beach have the opportunity to be promoted as a functional food, health ingredients to overcome free radicals or food preservatives. The antioxidant activity of mixed microalgae polysaccharides from Glagah and East Java was included in the active/moderate category, with IC50 value of 125.21µg/mL and 127.11µg/mL, respectively, while the antioxidant activity of polysaccharide S. platensis was low, 171.82µg/mL.
ACKNOWLEGEMENTS:
The funding from the Institute for Research and Community Service Universitas Airlangga with research grants: Indonesia Research Collaboration – World Class University 2020, No: 248/UN3.14/PT/2020.
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Received on 10.01.2023 Modified on 28.03.2023
Accepted on 04.05.2023 © RJPT All right reserved
Research J. Pharm. and Tech 2024; 17(1):277-283.
DOI: 10.52711/0974-360X.2024.00043