A REVIEW OF PHARMACOLOGICAL ACTIVITY OF MARINE ALGAE IN INDIAN COAST

A REVIEW OF PHARMACOLOGICAL ACTIVITY OF MARINE ALGAE IN INDIAN COAST

Ankita Sharma ^*, Raju Koneri and Deepak Kumar Jha

Department of Pharmacology, Karnataka College of Pharmacy, Bengaluru - 560064, Karnataka, India.

ABSTRACT: Indian coastline stretches about 5700 km covering 9 states on the mainland and about 7500 km including islands and union territories. Seaweeds, a renewable natural resource, found growing in large quantities along the Indian coast. Seaweeds are currently worldwide interest in finding new and safe promising organisms for health. It is one of the important essential producers of biomass in the marine environment. Seaweeds are not only of high ecological but also of great economic importance as they produce a wide variety of chemically active metabolites in their surroundings. The potential uses of algal biomass for the benefit of mankind have been intensively reviewed in the last few years. Marine algae have been used as a novel food with potential nutritional benefits in industry and medicine for various purposes. Furthermore, marine algae have shown to provide a rich source of natural bioactive compounds with antidiabetic, hepatoprotective, antiviral, antifungal, antibacterial, antioxidant, anti-inflammatory, anti-hypercholesterolemia and hypolipidemic and antineoplastic properties, etc. The present review is focusing on the bioactivities and potential pharmacological activity of marine algae which are found on the Indian coast.

Seaweeds, Marine algae, Pharmacological activity and Indian coast

INTRODUCTION: In modern medicine, no satisfactory effective therapy is yet available. Marine algae compounds have contributed to the global search for novel medicinal agents. In recent years, a significant number of novel metabolites with potent pharmacological properties have been discovered from the marine organism. Marine algae are one of the richest sources of structurally diverse natural products ^1-3. An increasing number of novel compounds have been isolated from marine algae, and many of them have been reported to possess interesting biological activities ^{4, 5}.

Marine algae or seaweeds have formed an important part of the diet of many eastern countries, and their use as food is well documented. Seaweed contains a range of components which have potential health benefits, and some have been demonstrated as potential chelators of heavy metals, Marine macro-algae are a primitive type of plants lacking true roots, stems and leaves and have been classified based on pigmentation into Phaeophyta (Brown), Rhodophyta (Red) and Chlorophyta (Green) types ⁶.

The marine algae are a rich natural resource of many biologically active compounds such as polyunsaturated fatty acids (PUFAs), sterols, proteins, polysaccharides, antioxidants, and pigments. They contain more than 60 trace elements in a concentration much higher than in terrestrial plants. They also contain protein, iodine, bromine, vitamins, and substances of stimulatory and antibiotic nature. Seaweeds are also traditionally consumed in different parts of the world. Many marine organisms live in complex habitats exposed to extreme conditions and, in adapting to new environmental surroundings, they produce a wide variety of secondary metabolites which cannot be found in other organisms. Numerous marine bioactive molecules have been identified, whose biological activities could interfere with the pathogenesis of many diseases ⁷.

Reported literature on the uses of seaweeds has been cited as early as 2500 years ago in China. Every year about 7.5-8 million tons of wet seaweeds is being produced along the coastal regions worldwide ⁸. The history of Indian seaweed research is not more than 75 years. The state of the Indian seaweed resources was last reviewed in 1998, and subsequently, a lot of new information relating to resources, utilization and commercial cultivation has been added. India (08.04–37.06 N and 68.07–97.25 E), a tropical South Asian country has a stretch of about 7500 km coastline, excluding its island territories with 2 million km² Exclusive Economic Zone (EEZ) and nine maritime states like Gujarat, Maharashtra, Goa, Karnataka, Kerala, Tamil Nadu, Orissa, Andaman and Nicobar, Lakshadweep Islands.

The seaweed flora of India is highly diversified and comprises mostly of tropical species, but boreal, temperate and subtropical elements have also been reported. In all, 271 genera and 1153 species of marine algae, including forms and varieties have been enumerated till date from the Indian waters ⁹.

TABLE 1: REPORTED SPECIES COMPOSITION ENCOUNTERED DURING DIFFERENT SURVEYS

*Qualitative survey only

Seaweeds differ from countries to countries. Cultivation conserves natural resources and improves the germplasm. Seaweed cultivation in India is still in the experimental stage they are collected manually from their natural habits. This harvesting is one of the important sources of livelihood to the coastal fisher-folk community. Seaweed collections are mainly centered along the southeastern coast of India from Rameswaram to Kanyakumari. There are about 25 agar industries and 10 align industries situated at different places in the maritime states of Tamil Nadu, Kerala, Karnataka, Andhra Pradesh, and Gujarat. Seaweeds are one of the foods yielding plants, which are found in lagoons and reed areas of coastal regions of India. The development of tissue culture techniques in seaweeds is essential for biotechnological application in strain improvement (Stevens & Purton, 1997). Seaweeds have a great value in providing low-cost nutrition and therapeutic protection almost everywhere in the world.

Marine algae are known to produce a wide variety of bioactive secondary metabolites, and several compounds have been derived from them for prospective development of novel drugs by the pharmaceutical industries. Now the red algae such as Gelidiella acerasa, Gracilaria edulis, G. crassa used for agar manufacture and brown algae Sargassum sp., Turbinaria sp. and Cystoseira sp. are used for alginates production (Anon 2004).

Marine algae are popular food ingredients in Asian countries. Studies have suggested that bioactive compounds isolated from marine organisms exhibit anti-cancer, anti-microbial, anti-fungal or anti-inflammatory and other pharmacological activities. Several algae have been found to have secondary metabolites most of which are a phenolic compound, which had medicinal potentials ^{19, 20}. Therefore, the aim of the present review was to facilitate discussion on the marine algae; the following review examines the existing scientific knowledge.

Bioactivities of Algae and Potential Use in Pharmacology:

Padina boergesenii (Brown Algae): Sudha et al., (2014) were reported antidiabetic activity ²¹, antioxidant activity ²², hepatoprotective activity ²³, chemo-preventive effects ²⁴ and herbivory effects ²⁵ of Padina boergesenii, Brown algae abundantly growing in Gulf of Mannar, southeast coast of Tamil Nadu, India. Oral administration of the Padina boergesenii to the STZ induced diabetic rats showed abridged effects on fasting blood glucose, insulin and lipoprotein levels. And also observed in liver glycogen and total protein levels in diabetic rats. The extract also significantly increased the activities of the key glycolytic enzymes like hexokinase, aldose, and phosphoglucoisomerase and decreased the activities of gluconeogenic enzymes like fructose-6-phosphatase and fructose-1, 6- diphosphatase in liver and kidney of diabetic rats.

Sargassum wightii (Brown Algae), Chaetomorpha linum (Green Algae) and Padina gymnospora (Light Brown Algae): Janarthanan S et al., (2012) was screened the antibacterial efficacy of various solvent namely; hexane, ethyl acetate, acetone and methanolic extracts for all three marine algae were tested against gram positive and gram negative human pathogenic bacteria using disc diffusion method. All three marine species were collected during low tide by hand-picking from the coast of Tuticorin, Tamil Nadu, India. And screened for antibacterial studies and were found that the acetone extracts of all the three marine algae showed higher inhibitory activity for the selected bacterial species than the other solvent extracts. And also revealed that among the three marine algae Padina gymnospora and Sargassum wightii were found to more active than Chaetomorpha Linum. ²⁶

Halimeda tuna (H. tuna), Turbinaria conoides (T. conoides) and Gracilaria foliifera (G. foliifera): Anantharaman P et al., (2011) was reported in-vitro antioxidant activities of three selected Indian seaweeds and were collected from South East Coast of India. The samples were used to determine the phenolic content, antioxidant activity and reducing power. Among the three seaweeds, Total phenolic content and total antioxidant activity were higher (1.231 ± 0.173 mg GAE/g, 1.675 ± 0.361 mg GAE/g in T. conoides and exhibited higher radical scavenging activity when compared to G. foliifera and H. tuna. Reducing the power of crude methanolic extract increased with concentrations of the extract and researcher concluded seaweeds could be considered for curing diseases of oxidative deteriorations ²⁷.

Laurencia brandenii (Red Algae): Selvin J et al., (2009) was observed cytotoxic potentials of red algae and specimens were collected from the habits of Kollam area located in the southwest coast of India. The red algae were extracted and fractionated in column chromatography using different solvent systems. The fractions were evaluated for brine shrimp cytotoxicity and hatchability assay using Artemia salina. The fatty acid composition of active fraction revealed that the main acid was 9, 12-Octadecadienoic acid (Z, Z) - (49.75%) followed by n-Hexadecanoic acid (14.24%) which might have functional role that confirmed by result at a dose of 200 µg/ml the active fraction of algae elicited 100% hatching inhibition, whereas in toxicity assay shown an LD₅₀ value of 93 µg/ml, which might have cytotoxic activity ²⁸.

Gracilaria edulis and Sargassum polycystum: Koneri et al., (2018) study were undertaken to evaluate antidiabetic activity of marine species in STZ induced diabetic rats. The marine algae were collected from the Mandapam coast (latitude 90 17’ Longitude 790 22, E), Gulf of manner, Tamil Nadu, India. The composition of active like; Carbohydrates, glycosides, phytosterol, proteins and the main bioactive phytochemical was phytosterol, which might have biological activities. And the results were marked an increase in total cholesterol, LDL cholesterol, and TG, while a significant decrease in HDL cholesterol level, was found in the diabetic control group. Hyperlipidemia is a known complication of diabetes mellitus and coexists with hyperglycemia and is characterized by increased level of cholesterol, TG and LDL cholesterol, and all the lipid abnormalities associated with diabetes was significantly normalized by treatment with the methanolic extract of algae of Sargassum polycystum and Gracilaria edulis. Algae also reported a significantly increase in beta cell density indicating property insulin secretohoge activity and this property may be due to regenerating activity on the beta cells ²⁹.

Sargassum ilicifolium (Brown Algae) Kappaphycus alvarezii: Yende SR et al., (2018) was screened anticonvulsant activity of brown algae in mice and an alga is a tropical and subtropical marine macroalgae collected from the inter-tidal rocky shore of Bhatkarwada, Ratnagiri coastal area of India. The researcher investigated the anticonvulsant activity of marine algae in maximal electroshock-induced convulsion and pentylenetetrazole (PTZ) induced convulsion and algae revealed the presence of alkaloids, terpenoids, Flavonoids, steroids, and saponin. The results of this study showed that chloroform extract (600 mg/kg) and ethanol extract (400 & 600 mg/kg) of algae significantly decreased the duration of tonic hind limb extension in maximal electroshock, as well as it significantly increased the latency to onset of convulsions in pentylenetetrazole model ³⁰.

Rebeca LJ et al., (2012) has reported antibacterial activity of Sargassum ilicifolium, Kappaphycus alvarezii and collected from different coastal regions of Rameshwaram (Southeastern coast of Tamil Nadu, India) were used in the present study. For microbiological testing of the seaweed extracts, agar well diffusion method was used.

The zone of inhibition was measured for all the different crude algal extracts against three strains of microorganisms namely, Escherichia coli, Salmonella sp. and Klebsiella sp. that cause diseases and disorders in human beings, animals and plants. Algae extracted prepared from chloroform, ethanol and methanol revealed a wide range of antibacterial activity against the mentioned pathogens. Researcher also revealed that maximum inhibition was noted with ethanol extracts in Sargassum ilicifolium rest all the extracts shown varied results in case of Kappaphycus alvarezii, the effect may be the bactericidal agents found in algae include amino acids, terpenoids, phlorotannins, acrylic acid, phenolic compounds, steroids, halogenated ketones and alkanes, cyclic polysulphides and fatty acids ³¹.

Gracilaria corticata: The Gracilaria corticata are generally considered to be important because of their pharmacological uses due to the presence of constituents like α-(1, 4)-3,6-anhydro-l-galactose and β-(1,3)-d-galactose ^{32, 33}. Deepa S et al., (2017) was reported to bioactivities of Gracilaria corticata algae which is one of the important species rich in various constituents responsible for various pharmacological activities.

The methanolic extracts of Gracilaria corticata rich in phenols and has higher percentage scavenging activity towards nitric oxide, hydroxyl radicals, hydrogen peroxide. The crude methanolic extracts of Gracilaria corticata was found to possess potent antimicrobial activity which was tested using well diffusion technique, and it also shows significant anticancer activity that was tested using various cancer cell lines like MCF7, normal VERO cell lines, and Hep-G2 by MTT assay ³⁴.

Movahedinia A et al., (2014) reported anti-oxidant properties of methanolic extracts of brown and red algae especially Gracilaria corticata was carried out by using ferric reducing ability of plasma (FRAP) method and diphenyl picrylhydrazyl (DPPH). And reported results, 50 mg/ml concentration both algae had no anti-oxidant activity with ABTS (μmol/g extract) and also there were no significant differences (p>0.05) between the studied algae in phenolic compounds and antioxidant activities that was tested by the DPPH and FRAP tests ³⁵.

Dist A et al., (2013) has reported the antioxidant of some seaweed constituents. They have reported antioxidant, anti-cholesterolemic and anti-tumor activity of ethanolic extract of Gracilaria corticata by performing antioxidant and cytotoxic potency of the in-vitro antioxidant assay using DPPH radical and reducing power ³⁶.

Rout S et al., (2015) has screened aqueous extract of Gracilaria corticata in diabetic rats was valued for two dissimilar doses such as 200 & 400 mg/kg by considering the method of blood glucose level, glycosylated hemoglobin, and hepatic glycogen level. And results revealed  aqueous extract of Gracilaria corticata drop blood glucose and glycosylated hemoglobin level in a dose dependent way and matched against the standard glipizide followed by the dose of 200 and 400 mg/kg showed 22.23 mg/g and 24.78 mg/g respectively in hepatic glycogen content which was ominously diminished by alloxan treated diabetic rats ³⁷.

Sampathkumar P et al., (2008) was investigated the hepatoprotective activity using aflatoxin B1 (AFB1) induced hepatotoxicity effect of marine algae Gracilaria corticata in contrast to AFB1 (1ppm) induced hepatic damage which were examined using important refereeing parameters like total protein content, weight of the liver albumin, body weight gain and tested along transaminase (SGOT and SGPT), lactate dehydrogenase (LDH) and alkaline phosphatase (ALP) as enzyme markers. And results revealed a decreased level of the above said parameters authenticated the Hepatic damage significantly (p<0.05) with the aqueous extract concentration of 250 mg kg-1 body weight ³⁸.

Gracilaria verrucosa (Red), Enteromorpha compressa (Green), Ulva fasciata (Green), Turbinaria conoides (Brown): Mohapatra L et al., (2016) the study was designed to evaluate the antioxidant, hypoglycemic and antidiabetic activities of different solvents extract viz. Petroleum ether, ethyl acetate and methanol extracts of these seaweeds. And the extracts were evaluated for total phenolic content, Reducing power, nitric oxide, and H₂O₂ scavenging tests. The extracts with superior antioxidant activity among these seaweeds were further tested hypoglycemic and antidiabetic activity. The IC₅₀ value of ethyl acetate of Ulva fasciata was found to be 123.39 and 127.65 μg/ml for H₂O₂ and NO free radical scavenging activity respectively. Total phenol content for ethyl acetate of Ulva fasciata was 207.23 ± 2.41 mg/g. Fasting plasma glucose level in normal mice was significantly (p<0.05) decreased even after 6 days of ethyl acetate of Ulva fasciata treatment at the dose 200 mg/kg. The area under the curve of oral glucose tolerance test was not affected significantly, though the considerable reduction in area under the curve was found in both ethyl acetate of Ulva fasciata 100 and 200 mg/kg treated groups. It was found that ethyl acetate of Ulva fasciata has potent in-vitro alpha-amylase inhibiting property when compared to the standard, acarbose. And results suggested that the anti-diabetic activity of U. fasciata may be due to its underlying antioxidant, hypoglycemic and alpha-amylase inhibiting property.

Presence of alkaloid was detected in Petroleum ether of Ulva fasciata. Gum and mucilage were detected in two green seaweed extracts (methanol extract of Ulva fasciata and methanol extract of Enteromorpha). Tannins, protein and amino acids were detected in methanol extracts of all seaweeds. Phenolic compounds were detected in ethyl acetate and methanol extracts of all seaweeds. Whereas, carbohydrate was absent in all the seaweed extracts ³⁹.

Acanthophora spicifera (Red), Padina tetrastomatica (Brown) and Caulerpa scalpelliformis (Green): Radhika D et al., (2015) the experiment was carried out for antidiabetic activity against alloxan-induced diabetic rats were collected from Tuticorin coast (08° 46’ 2.15”N lat; 78°11’ 16.05” E long) and fully grown & submerged underwater from the tidepools. In diabetic control rat, liver glycogen content decreased significantly by 79.89 % as compared to non-diabetic control. Seaweed extracts of A. spicifera, P. tetrastomatica, and Caulerpa scalpelliformis at a dose 200 mg/kg led to 74.47%, 66.05%, 68.79% and 70.56% increase in liver glycogen content in compared to diabetic control group. And also revealed that mean level of enzymes Hexokinase, Glucokinase and substrate Glucose-6-phosphatase values decreased in diabetic control. The respective percentage decrease was 56.19%, 79.96% and 67.69% in diabetic control.

Treatment with extracts of A. spicifera, P. tetrastomatica, and Caulerpa scalpelliformis led to rising in the percentage of these parameters by 22.03% and 56.03%, 45.21% and 34.28%, 67.78% and 47.5% and 33.33%, 67.88% and 45.76% respectively (p<0.001) as compared to diabetic control. There were no statistically significant differences were seen in the mean WBC, and RBC counts, HB and Platelet values as compared to the non-diabetic animals ⁴⁰.

Acanthophora specifera: Kumar RR et al., (2015) has reported in-vitro antioxidant efficacy and antimutagen on selected algae. And they were collected from Mandapam Coastal Area, Rameswaram Tamil Nadu, India. The algae revealed the presence of saponin, tannin, Flavonoids, steroids, terpenoids, alkaloids, amino acid, polyphenol, anthraquinones, and glycosides.

Different concentrations of Acanthophora specifera (20, 40, 60 and 80 μg/ml) were chosen for in-vitro antioxidant activity and standard L-Ascorbic acid was used. Results were demonstrated in vitro antioxidant property of Acanthophora specifera in respect to DPPH radical scavenging assay, Hydroxyl radical scavenging assay, Superoxide anion scavenging assay, nitric oxide scavenging assay, Fe²⁺ chelating assay, Reducing power assay and studied was suggested that the algae might have an antioxidant, anti-allergic, anti-inflammatory, anti-microbial, anti-cancer activity due to the presence of mentioned bioactive chemicals.

Gelidiella acerosa: Syad AN et al., (2012) was assessed of anticholinesterase (AChE), and butyryl-cholinesterase (BuChE) activities of algae⁴² were collected from the South Indian coastal area, Tamil Nadu and inhibitory activities were analyzed by spectrophotometric method. Benzene and ethyl acetate extract showed positive results for the presence of terpenoids, cardiac glycosides, alkaloids, and tannins. The results showed that, at 487.80 μg/mL, benzene extract showed significant (p<0.05) inhibitory activity against both AChE and BuChE with the percentage of inhibition 54.18 ± 5.65% (IC₅₀ = 434.61 ± 26.53 μg/mL) and 78.43 ± 0 % (IC₅₀ = 163.01 ± 85.35 μg/mL), respectively. The mode of inhibition exhibited by benzene extract against the AChE and BuChE was found to be the competitive and uncompetitive type of inhibition. GC-MS illustrates that the benzene extract possesses a high amount of terpenoids, which could be the reason for potential cholinesterase inhibitory activity.

Several marine algae’s like; Caulerpa racemosa, Codium capitatum, Ulva fasciata, Halimeda cuneata, Amphiora ephedraea, Amphiora bowerbankii, Dictyota humifusa, Hypnea valentiae, Padina gymnospora, Ulva reticulate, Gracilaria edulis, Ecklonia stolonifera, Ishige okamurae

Kim SK et al., (2011) was mentioned in their review paper, the above several marine algae’s of methanolic extracts which have potential Acetylcholinesterase inhibitory activities ⁴³. The inhibition of acetylcholinesterase (AChE) enzyme, which catalyzes the breakdown of ACh, may be one of the most realistic approaches to the symptomatic treatment of Alzheimer’s disease, which is known for an irreversible, progressive neurodegenerative disease and resulting in memory loss, behavior disturbances and decline the standard of life.

Syncephalastrum racemosum and Gracilaria corticata: Ushasri R et al., (2015) has reported invitro antidiabetic activity of ethanolic and acetone extracts of endophytic fungi of marine algae by alpha-amylase inhibition assay method.⁴⁴ the study was aimed at screening the diabetic ant activity of endophytic fungi isolated from Gracilaria corticata. Seaweed was processed, placed on potato dextrose agar (PDA) medium and Sabourds Dextrose Agar (SDA) medium respectively. The mycelial growth of S. racemosum was inoculated into Potato Dextrose Broth (PDB) and allowed for fermentation. The mycelial mat was extracted with acetone and ethanol. The crude extracts of fungi showed the highest inhibitory activity of 23.7% and 19.4%.

Brown seaweed: Cystoseirra sp, Dictyopteris sp, Dictyota, Hormophysa, Hydroclathrus, Padina, Sargassum, and Turbinaria is maximally fulfilled from Asian countries viz. Korea, Japan, China. Brown alga is a rich source of bioactive components like phlorotannins, polyphenols, pigments, sulfated polysaccharides, vitamins (A, B, C, and E), dietary fibers, omega-3 fatty acids, and essential amino acids. The anti-diabetic potential of brown algae is maximally due to polyphenols, polysaccharides, and pigments. Phlorotannins show α-glucosidase, α-amylase, and PTP inhibitory functions. The phlorotannins were found to enhance peripheral glucose utilization by activating glucose transporter sub-type 4 (GLUT-4) and activation of the protein kinase (AMPK) pathway. Fucoxanthin is a marine carotenoid present in brown marine seaweeds.

It induces the synthesis of docosahexaenoic acid (DHA) in the liver. Fucoxanthin reduces white adipose tissue fat accumulation and promotes weight loss. With 0.02% dose fucoxanthin there is a significant lowering of body weight. Fucoxanthin also helps to lower plasma and hepatic triglyceride concentrations. Adipocyte fatty acid synthesis, hepatic fatty acid, and triglyceride synthesis are also lowered by fucoxanthin.

Animal experimentations have shown that it slows down fasting blood glucose level and modulates plasma-insulin level in obese mice. Fucoxanthin controls insulin resistance, inhibits adipokines, TNF-α, monocyte chemoattractant protein-1(MCP-1), IL-6.

TABLE 2: COMPILED DATA ON MARINE ALGAE WITH PHARMACOLOGICAL ACTIVITY

CONCLUSION: Marine algae biodiversity needs systematic study. In this review, we were able to show that these all marine algae of Indian coast and the most probable reason for their potential activity might be related to the presence of different bioactive compounds in marine algae, and are easily extracted with solvents can be used for development of drugs in the pharmaceutical industries. The significance of these marine algae’s need to further characterize, and they will be evaluated for their bioavailability. However, corrective measures like scientific research, education, conservation, and awareness are essential to increase the use of marine algae.

ACKNOWLEDGEMENT: The author is grateful to the Department of Pharmacology, Karnataka College of Pharmacy, Bangalore, India for their support and useful discussions with Dr. Raju Koneri and Mr. Deepak Kumar Jha.

CONFLICT OF INTEREST: We declare that we have no conflict of interest.

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    How to cite this article:

    Sharma A, Koneri R and Jha DK: A review of pharmacological activity of marine algae in Indian coast. Int J Pharm Sci & Res 2019; 10(8): 3540-49. doi: 10.13040/IJPSR.0975-8232.10(8).3540-49.

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