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Year : 2012  |  Volume : 11  |  Issue : 2  |  Page : 99-108

Phycochemistry of some Sargassum spp. and their cytotoxic and antimicrobial activities

Pharmacognosy Department, Pharmaceutical and Drug Industries Research Division, National Research Centre, Cairo, Egypt

Date of Submission12-Mar-2012
Date of Acceptance30-Aug-2012
Date of Web Publication18-Jul-2014

Correspondence Address:
Azza A Matloub
Pharmacognosy Department, Pharmaceutical and Drug Industries Research Division, National Research Centre, El-Bohouth St., 12311 Dokki, Cairo
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Source of Support: None, Conflict of Interest: None

DOI: 10.7123/01.EPJ.0000419800.62958.79

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A comparative study on the chemical composition as well as cytotoxic and antimicrobial activities of the brown algae Sargassum asperifolium, Sargassum dentifolium, and Sargassum linifolium (family: Sargassaceae) from the Red Sea, Hurghada, Egypt, is carried out.


The volatile constituents obtained by hydrodistillation as well as the isolated unsaponifiable matter and the fatty acids were analyzed using the gas chromatography/mass spectrometry technique. Antitumorigenic activities of the crude extracts of the three algae have been evaluated in vitro on different human cell lines. Furthermore, the antimicrobial activities of the volatile constituents, successive extractives, unsaponifiable matter, and fatty acids have been tested on 11 different microorganisms.


The analysis of the volatile fraction led to the identification of sexual pheromones, terpenes, phenolic compounds, free fatty acids, and esters. The most abundant sterols of unsaponifiable matter were fucosterol and cholesterol in all algae. Palmitic acid was found in all investigated algae as a major fatty acid. Biological screening proved that the tested algae have various cytotoxic and antimicrobial activities.


S. asperifolium, S. dentifolium, and S. linifolium are rich in cytotoxic and antimicrobial bioactive metabolites.

Keywords: antimicrobial activity, cytotoxic activity, Sargassum asperifolium , Sargassum dentifolium , Sargassum linifolium

How to cite this article:
Matloub AA, Awad NE. Phycochemistry of some Sargassum spp. and their cytotoxic and antimicrobial activities. Egypt Pharmaceut J 2012;11:99-108

How to cite this URL:
Matloub AA, Awad NE. Phycochemistry of some Sargassum spp. and their cytotoxic and antimicrobial activities. Egypt Pharmaceut J [serial online] 2012 [cited 2021 Oct 19];11:99-108. Available from:

  Introduction Top

Marine natural resources are a treasury of a large group of structurally unique secondary metabolites useful to medicine, which have yielded a large number of drug candidates 1.

The anticarcinogenic properties of brown seaweeds are well known in some cultures such as traditional Chinese medicine 2 and in ancient Ayurvedic texts 3. In addition, they are mentioned in the Ebers Papyrus of the ancient Egyptians, who used seaweed to treat breast cancer 4.

There are numerous reports on compounds that have been derived from Sargassum spp. with a broad range of biological activities. Patra and colleagues, 2007, reported that the methanol extract of Sargassum spp. showed strong antioxidant activity and had antimicrobial activity against Gram-positive and Gram-negative bacteria 5. Further, the methanol extract of Sargassum swartzii had chronic and acute anti-inflammatory effects 6, whereas the methanol extract of Sargassum henslowianum and Sargassum siliquastrum and the ethanol extract of Sargassum dentifolium acted as antidotes against the hepatotoxicity induced by carbon tetrachloride 7,8. Other studies have reported that the hot water extract of Sargassum horneri is the most potent anticoagulant and has a high activated partial thromboplastin time 9, and that polysaccharides isolated from Sargassum trichophyllum show antiviral activity against herpes simplex virus type 2 10.

Tang et al. 11 isolated several sterols from Sargassum carpophyllum that showed various cytotoxic activities against several cancer cell lines. Moreover, farnesy-lacetones isolated from S. siliquastrum showed a moderate vasodilatation effect on the basilar arteries 12. Chandraraj et al. 13 reported that the ethyl acetate fraction of Sargassum ilicifolium stimulated in-vitro chemotatic, phagocytic, and intracellular killing of human neutrophil immunostimulants and showed prominent immunostimulator activity in vivo. S. siliquastrum acts as a food preservative that reduces the microbial count of bread and increases the time of storage 14.

The hydroalcoholic extracts of Sargassum asperifolium, Sargassum dentifolium, and Sargassum linifolium have shown various insecticidal and antiviral activities in vitro on isolated cell lines of Spodoptera littoralis (Sl52 cells) and Spodoptera frugiperda (Sf9 cells) with or without inoculation of nucleopolyhedrovirus and in vivo on S. littoralis nucleopolyhedrovirus replication 15. Furthermore, Aboutabl et al. 16 have reported that the different extracts of S. dentifolium, collected from the Mediterranean coast of Egypt, showed potential insecticidal activity against S. littoralis at different stages of the life cycle.

Numerous substances such as 24-vinylcholest-4-ene-24-ol-3-one, saringosterone, saringosterol, and a hydroazulene diterpene dictyone were isolated from S. asperifolium 17. Abdel-Fattah et al. 18 isolated sargassan (a sulfated heteropolysaccharide) from S. linifolium and Aboutabl et al. 16 isolated diisooctyl phthalate from S. dentifolium.

Other constituents such as pheromones 19, phlorotannins 20, polyphenols, benzoquinone, hydroquinones with a diterpenoid side chain, cyclopentenones, bisnorditerpene derivatives 21, and phthalic acid derivatives 22,23 have been isolated from different Sargassum spp.

The current literature and the lack of the data and information on the composition of the volatile matter and other active constituents of S. asperifolium, S. dentifolium, and S. linifolium led us to isolate and identify their volatile constituents and lipoidal matter. During our search for active cancer chemoprotective agents in these marine algae, we also evaluated the volatile constituents, successive extracts, and unsaponifiable and saponifiable matter as antimicrobial agents.

  Materials and methods Top

Thallus material

The three brown algae S. asperifolium (Hering and G. Martens ex J. Agardh), S. dentifolium (Agardh), and S. linifolium (C. Agardh) (family: Sargassaceae) were collected at about 2–4 ft under the water surface on the Red Sea coasts in Hurghada, Egypt, during May 2007 and authenticated by Prof. S.A. Shaalan, Faculty of Science, Alexandria University.

Preparation of crude extract

In total, 100 g of the air-dried powdered thallus from each collected sample was extracted successfully with 70% methanol. Each extract was filtered and evaporated under vacuum.

Preparation of successive extracts

In total, 100 g of the air-dried powdered thallus from each collected sample was extracted exhaustively with petroleum ether (40–60°C), ether, chloroform, ethyl acetate, and methanol in a Soxhlet apparatus, followed by maceration in water. Each extract was filtered, evaporated under vacuum, and weighed.

Isolation of the volatile constituents

Pure and fresh homogenized algae (1 kg) were hydrodistilled in a modified Likens–Nickerson apparatus 24 using n-pentane (AR grade). The n-pentane layer was evaporated under pressure to yield a pale-yellow oil.

Isolation of lipoidal matter

Each petroleum ether residue was saponified using 0.5 N alcoholic KOH. The unsaponifiable matter was extracted with ether, washed with water, dried over anhydrous sodium sulfate, evaporated to dryness, weighed, and analyzed by gas chromatography/mass spectrometry (GC/MS). The fatty acids were liberated by acidification of the saponifiable matter and then extracted with ether and dried in vacuo. The fatty acids obtained were methylated (MeOH, 4–5% dry H2SO4) to yield the methyl ester derivatives and then analyzed by GC/MS.

Gas chromatography/mass spectrometry analysis

GC/MS analysis was carried out using a Finnigan SSQ 7000 (ThermoFinnigan, San Jose, California, USA) GC/MS spectrophotometer equipped with library software Wiley 138 and NBS 75 under the following conditions: DB-5-fused silica capillary column, 30 m in length, 0.32 mm ID, and with a film thickness of 0.25 μm; carrier gas, helium at a flow rate of 10 ml/min; temperature programmed to 60–260°C at a rate of 4°C/min (volatile constituents), 70–290°C at a rate of 5°C/min (unsaponifiable matter), 60–220°C at a rate of 4°C/min (fatty acid methyl ester derivatives), chart speed: 0.5 cm/min, ionization voltage 70 eV, and detector: flame ionization detector.

The identification of the constituents was carried out depending on the fragmentation of the spectra obtained and by comparing them with those of available authentic standards such as an alkane standard mixture, hexadecanol, palmitic acid, geranylgeraniol, α-copanene, longifolene, aromadendrene, D-limonene, caryophyllene, germacrene D, phytol, β-ionone, cholesterol, campesterol, stigmasterol, β-sitosterol, fucosterol, and ergosterol (Sigma-Aldrich Chemie GmbH, Germany). In addition, brassicasterol, 22-dehydrocholesterol, fucostenone, clerosterol, and avensterol have been isolated previously and identified by our research group at the Pharmacognosy Department, NRC, Egypt, or by published data 25–28, and a library database [Wiley (Wiley Institute, USA) and NIST (National Institute of Technology, USA)]. Quantitative determination was carried out on the basis of peak area measurements of the GC chromatograms.

Antitumor activity


Authentic culture, H460 (lung carcinoma human cell line), Hela (cervix carcinoma human cell line), HepG2 (liver carcinoma human cell line), Mcf7 (breast carcinoma human cell line), Molt4 (leukemia carcinoma human cell line), and U251 (brain carcinoma human cell line) were obtained from the American Type Culture Collection, USA.

Culture media

The cells were suspended in RPMI 1640 medium supplemented with 10% fetal calf serum, 1% antibiotic–antimycotic mixture (10 000 U/ml K-penicillin, 10 000 μg/ml streptomycin sulfate, and 25 μg/ml amphotericin B), and 1% L-glutamine (all purchased from Lonza, Braine-l'Alleud, Belgium).

Assay method for cytotoxic activity

The cytotoxicity against H460, Hela, HepG2, Mcf7, Molt4, and U251 was determined at the National Cancer Institute, according to the method used by Skehan et al. 29. Adriamycin (Doxorubicin; Pharmacia, Stockholm, Sweden) 10 mg vials were used as the reference drug.

The cell lines were plated in 96-multiwell plates (104 cells/well) for 24 h before treatment with the tested samples to allow the attachment of cells to the wall of the plate. Then, a 50 μl aliquot of serial dilutions of the crude extract (1.0, 2.5, 5, and 10 μg/ml) was added and the plates were incubated for 48 h at 37°C in a humidified incubator containing 5% CO2 in air. Triplicate wells were prepared for each individual dose. Cells were fixed, washed, and stained with sulforhodamine B stain (Sigma, USA). Excess stain was washed with acetic acid and the attached stain was recovered with Tris EDTA buffer (Sigma, USA). The color intensity was measured in an ELISA reader spectrophotometer (Tecan Group Ltd.-Sunrise, Mannedorf, Switzerland).

Microbiological activity

The antimicrobial activity of the volatile constituents, successive extracts, saponifiable matter, and fatty acids of algae examined was determined against that of several microbes using the antibiotic assay method 30. Pure strains of bacteria, yeasts, and fungi were kindly provided by the Microbial Genetics Department, National Research Center, Egypt. The bacterial strains used were Bacillus cereus (Gram positive, G+), Bacillus subtillis (G+), Staphylococcus aureus (G+), Escherichia coli (Gram negative, G), Pseudomonas aeruginosa (G), and Pseudomonas fluorescens (G). The yeast strains were Saccharomyces carles and Saccharomyces cerevisiae, whereas the fungi were Aspergillus flavus, Aspergillus niger, and Diplodia oryzea.

The bacteria were cultured on Lauria–Bertani Medium 31, whereas the yeast strains were cultivated on Yeast Extract Peptone Medium 32. The fungi were cultured on Potato-Dextrose Agar growth medium 33. The oils, successive extracts, unsaponifiable matter, and fatty acids were sterilized by filtration through a bacterial membrane filter (0.45 μm, 2.5 mm diameter; Millipore, Billerica, Massachusetts, USA). A concentration of 100 μg/disc was used. The discs (6 mm diameter), after being air dried, were firmly applied to the surface of inoculated agar plates. The diameters of inhibition zones were measured per applied disc after incubation at 37°C for 24 h with the bacteria strains, whereas those containing yeast and fungi were incubated at 30°C for 48–72 h. Amoxycillin (Medical Union Pharmaceuticals Co., Ismailia, Egypt) as an antibacterial agent (100 μg/disc) and canesten (Alexandria Co., Alexandria, Egypt) as an antifungal agent (100 μg/disc) were used as reference drugs.

Statistical analysis of data

All values were expressed as means, with three replicates for each treatment. Data were subjected to a paired sample t-test using SPSS (version 17.0; SPSS Inc., Chicago, Illinois, USA). P less than 0.05 was considered as significant.

  Results and discussion Top

The yields of volatile oils of fresh algae S. asperifolium, S. dentifolium, and S. linifolium were 0.038, 0.041, and 0.043% (w/w), respectively.

Fifty-seven, 53, and 54 compounds were identified, which represent 93.93, 92.36, and 89.43% of the total volatile compounds released from S. asperifolium, S. dentifolium, and S. linifolium; respectively. [Table 1] shows that the volatile constituents of the algae are composed of alcohol (15.74, 16.44, and 15.76 %), aldehyde (−, 0.25 and 0.09%), esters (27.98, 29.05, and 10.08%), free acids (6.17, 9.43, and 1.85%), halogenates (0.33, 0.22, and 0.25%), C11 hydrocarbon pheromones (2.34, 5.89, and 24.38%), sesquiterpenes (1.31, 3.44, and 0.72%), hydrocarbons (28.28, 22.95, and 26.36%), ketones (11.43, 2.75, and 9.72%), and miscellaneous compounds (0.35, 1.94, and 0.22%), respectively.
Table 1: Chemical composition of the volatile constituents of brown algae Sargassum asperifolium, Sargassum dentifolium, and Sargassum linifolium

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Dictyopterene Dº, which is an odoriferous C11 hydrocarbon, was a major constituent in S. linifolium (20.26%) and was also identified in the oil of S. asperifolium and S. dentifolium. Another C11 hydrocarbon pheromone dictyopterene C was detected in S. asperifolium; dictyopterene A was detected in S. dentifolium and S. linifolium. These hydrocarbons have been detected here for the first time in S. asperifolium, S. dentifolium, and S. linifolium. However, ectocarpene and dictyotene have been detected previously in S. asperifolium 34.

Characteristic aroma dictyopterenes have been identified as constituents of brown algae with male gamete-attracting activity 19.

Bis-2-ethylhexyl phthalate was identified as the principal constituent in S. asperifolium and S. dentifolium (24.25 and 25.28%, respectively), and this was also found in the Sargassum wightii 22, S. dentifolium 16, and Sargassum spp. 23. The biosynthesis of di-(2-ethylhexyl) phthalate by red alga Bangia atropurpurea has been described by Chen 35. Furthermore, di-(2-ethylhexyl) phthalate showed antimicrobial activity against various microorganisms 36, antileukemic and antimutagenic 14. In addition, dibutyl phthalate has been detected in some edible brown algae such as Undaria pinnatifida and Laminaria japonica as a natural product 37.

Furthermore, sesquiterpenoid compounds α-copaene, β-bourbonene, longifolene, γ-elemene, aromdenderene, and muurola-4(14),5-diene have been detected for the first time in Sargassum spp. under study. These compounds were detected in Dictyopteris spp. 38. β-Ionone was detected in all algae under investigation, and it has antibacterial and antifungal activity 39. Two aliphatic chains diterpenes, phytol and geranylgeraniol, were identified in the tested algae, which had bactericidal activity against S. aureus. These diterpenes exerted both growth-inhibitory and growth-accelerating effects depending on their concentration 40.

The yields of unsaponifiable matter of S. asperifolium, S. dentifolium, and S. linifolium were 0.22, 0.22, and 0.61% (w/w), respectively. Fifty-seven, 44, and 40 compounds were identified, which represent 82.17, 79.74, and 80.44% of the total unsaponifiable matter of S. asperifolium, S. dentifolium, and S. linifolium, respectively. [Table 2] shows that the unsaponifiable matter of S. asperifolium, S. dentifolium, and S. linifolium is composed of sterols (51.27, 22.23, and 32.35%), which represent the mean fraction of unsaponifiable matter, alcohol (7.01, 14.87, and 7.15%), aldehydes (0.27, 0.11%, and –), esters (3.58, 14.01, and 10.46%), hydrocarbons (15.87, 4.98, and 5.48%), ketones (0.43, 3.21, and 5.91%), phenols ( 2.03, 19.64, and 18.45%), and miscellaneous compounds (1.71, 0.69, and 0.64%).
Table 2: Chemical composition of the unsaponifiable fraction of the brown algae Sargassum asperifolium, Sargassum dentifolium, and Sargassum linifolium

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Fucosterol was detected as a major sterol in the algae tested as other Sargassum spp. showed cytotoxic activity against various carcinoma human cell lines 11,41. In addition, it showed antifungal activity against Curvularia lunata, Stachybotrys atra, and Microsporum canis. These results were obtained for the first time in this work for unsaponifiable matter from Sargassum spp.

The percentages of fatty acids of the brown algae S. asperifolium, S. dentifolium, and S. linifolium were 0.09, 0.041, and 0.043% (w/w), respectively. [Table 3] shows that the saturated fatty acids represent the main fraction (56.12, 65.39, and 56.42%, respectively) of fatty acid, and palmitic acid was found in all Sargassums spp. under study as a major fatty acid. Furthermore, oleic acid represents the main unsaturated fatty acid of S. dentifolium and S. linifolium. However, 9,12-octadecadienoic acid represents the major unsaturated fatty acid of S. asperifolium.
Table 3: Methyl ester of the fatty acid composition of the brown algae Sargassum asperifolium, Sargassum dentifolium, and Sargassum linifolium

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Cytotoxic activity

The cytotoxic activity of crude extracts of Sargassum spp. under study against human cells H460, Hela, HepG2, MCF7, Molt4, and U251 cultured in vitro was examined. The percentages of inhibition and relative inhibition related to the reference drug doxorubicin are shown in [Table 4] and [Table 5] and illustrated in [Figure 1], [Figure 2] and [Figure 3]. The crude extract of S. linifolium has significantly promising in-vitro cytotoxic activity against HepG2 and Molt4, with an effective dose (ED50) of 5.97 and 2.28 μg/ml, respectively, compared with the control, and at concentrations of 5 and 10 μg/ml, they showed good cytotoxic activity against HepG2, which was comparable to that of the reference drug doxorubicin.
Figure 1: Cytotoxic activity of a crude extract of Sargassum asperifolium on different human cell lines.

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Figure 2: Cytotoxic activity of a crude extract of Sargassum dentifolium on different human cell lines.

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Figure 3: Cytotoxic activity of a crude extract of Sargassum linifolium on different human cell lines.

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Table 4: Cytotoxic activity of the crude extract of the brown algae Sargassum asperifolium (S1), Sargassum dentifolium (S2), and Sargassum linifolium (S3) against different cultured human cell lines

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Table 5: Relative inhibition of growth of different human cell lines related to doxorubicin

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Whereas the crude extract of S. dentifolium showed significant cytotoxic activity against HepG2 with an ED50 of 11.03 μg/ml, H460 and MCF7 related to the control test and at concentrations of 5 and 10 μg/ml showed good cytotoxic activity against H460 in comparison with doxorubicin.

Furthermore, the crude extract of S. asperifolium at a concentration of 1 μg/ml showed high cytotoxic activity against H460, whereas it showed good cytotoxic activity at concentrations of 1 and 2.5 μg/ml against U251 and H460, respectively, when compared with doxorubicin as a reference drug.

It is noteworthy that the authors have isolated many bioactive cytotoxic constituents such as diterpenes and polysaccharides from different marine algae 42–44. Khanavi et al. 41 found that fucosterol, the most abundant phytosterol in the brown algae, is responsible for the cytotoxic effect against a breast carcinoma cell line [inhibitory concentration (IC50) 27.94 μg/ml] and a colon carcinoma cell line (IC50 70.41 μg/ml).

The antimicrobial activity

The antimicrobial activities of the volatile constituents, successive extracts, unsaponifiable fractions, and fatty acids fractions of Sargassum spp. under study are summarized in [Table 6]. The different fractions of S. asperifolium showed significant antimicrobial activity against B. cereus compared with amoxycillin as a reference drug. However, the various fractions of S. dentifolium showed pronounced antimicrobial activity against S. carles compared with canesten as a reference drug. Ether, ethyl acetate, and methanol fractions of S. linifolium were found to have potent antimicrobial activities against D. oryzea when compared with standard canesten.
Table 6: Inhibitory response of the different fractions of the brown algae Sargassum asperifolium (S1), Sargassum dentifolium (S2), and Sargassum linifolium (S3) on the tested microbes in comparison with standard antibacterial and antifungal substances

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It has been reported that the antimicrobial activity of some algal species is because of the presence of a mixture of fatty acids such as capric, lauric, linoleic, myristic, oleic, palmitic, and stearic acid 45. It is clear from the present study that these fractions can be utilized as good natural antimicrobial agents in the pharmaceutical industry.

  Conclusion Top

The volatile constituents as well as unsaponifiable matter and fatty acids isolated and identified from S. asperifolium, S. dentifolium, and S. linifolium, collected from the Red Sea coasts in Hurghada, for the first time comprise alcohol, aldehydes, esters, free acids, halogenates, C11 hydrocarbon pheromones, sesquiterpenes, hydrocarbons, and ketones. The different extracts of these three algae have various antimicrobial and cytotoxic activities and can act as promising natural sources of these bioactive products.[45]

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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


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