Evaluation of cytotoxic and antibacterial properties of Symbiodinium sp. isolated and purified from Stichodactyla haddoni in the Persian Gulf and Gulf of Oman

Document Type : Research Paper

Authors

1 Ph.D. in Marine Biology, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran

2 Professor in Department of Biology, Faculty of Science, University of Qom, Qom, Iran

3 Associate Professor in Department of Marine Biology, Faculty of Marine Science, Tarbiat Modares University, Noor, Iran

4 Assistant Professor in Department of Marine Biology, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran

Abstract

Symbiotic relationships play an important role in marine ecosystems. Among marine symbionts, marine dinoflagellate chemical compounds have drawn the interest of biologists and ecologists due to their rich supplies of unique active secondary metabolites. The aim of this study was to evaluate the cytotoxicity and antibacterial activity of Symbiodinium sp. extract isolated and purified from Stichodactyla haddoni in the Persian Gulf and the Gulf of Oman and purified and cultured Symbiodinium sp. in vitro. Sea anemone samples of S. haddoni were collected during summer and winter and Symbiodinium sp. was isolated from anemones by manual homogenization method and then cultured and extracted. Brine shrimp lethality test was used for investigation of Symbiodinium sp. extracts toxicity. The effect of extracts on human pathogenic bacteria, Escherichia coli and Staphylococcus aureus was also investigated. Results showed that the cytotoxicity of Symbiodinium sp. extracts during 24 and 72 hours showed the highest cytotoxicity in Chabahar summer with less LC50 (0.179 and 0.075 mg/mL, respectively). Comparison of antibacterial properties showed that the highest zone of inhibition was related to winter in Qeshm Island, but it was less than the penicillin zone. In general, the study of methanolic extracts did not show antibacterial properties, while they showed lethal effects on A. salina. Therefore, Symbiodinium sp. can be used as more specific anti-cancer and anti-tumor tests as a cytotoxic dinoflagellate.

Keywords


طهماسبی م.ح. و زارعی دارکی ب. 1396. اندازه‌گیری نرخ رشد ویژه‌ی داینوفلاژله Symbiodinium sp. جداسازی شده از شقایق دریایی Stichodactyla haddoni. مجله بوم شناسی آبزیان، ۷(۲) : ۱۱۴-۱۰۶.
Camacho F.G., Rodríguez J.G., Miron A.S., Garcia M.C., Belarbi E.H., Chisti Y. and Grima          E.M. 2007. Biotechnological significance of toxic marine dinoflagellates. Biotechnology Advances, 25(2): 176–194.
Chang S.S., Prezelin B.B. and Trench R.K. 1983. Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Marine Biology, 76(3): 219–229.
De Jesus Raposo M.F., De Morais A.M.B. and De Morais R.M.S.C. 2015. Marine polysaccharides from algae with potential biomedical applications. Marine Drugs, 13(5): 2967–3028.
Dubinsky Z.V.Y. and Stambler N. 1996. Marine pollution and coral reefs. Global Change Biology, 2(6): 511–526.
Ebrahimi Nigjeh S., Yusoff F.M., Mohamed Alitheen N.B., Rasoli M., Keong Y.S. and Omar A.R.B. 2013. Cytotoxic effect of ethanol extract of microalga, Chaetoceros calcitrans, and its mechanisms in inducing apoptosis in human breast cancer cell line. BioMed Research International, 2013: 1–8 (783690)
Ferrara L. 2020. Dinoflagellates important marine producers of natural bio-compounds with high biotechnological and pharmacological potential. Journal of Food Chemistry and Nanotechnology, 6(3): 138–149.
Finney D.J. 1971. Probit Analysis. Cambridge University Press,UK. 333P.
Fusetani N. and Kem W. 2009. Marine Toxins as Research Tools, Vol.: 46. Springer Science and Business Media, Germany. 259P.
Guillard R.R. and Ryther J.H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 8(2): 229–239.
Jeffrey S.W. and Haxo F.T. 1968. Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. The Biological Bulletin, 135(1): 149–165.
Kim S.K. 2015. Handbook of Marine Microalgae: Biotechnology Advances. Academic Press, USA. 1512P.
Kobayashi J., Ishibashi M., Nakamura H., Hirata Y., Yamasu T., Sasaki T. and Ohizumi Y. 1988. Symbioramide, a novel Ca2+-ATPase activator from the cultured dinoflagellate Symbiodinium sp. Experientia, 44(9): 800–802.
Kobayashi J.I. and Tsuda M. 2004. Amphidinolides, bioactive macrolides from symbiotic marine dinoflagellates. Natural Product Reports, 21(1): 77–93.
Kobayashi J.I., Ishibashi M., Nakamura H., Ohizumi Y., Yamasu T., Hirata Y., Sasaki T., Ohta T. and Nozoe S. 1989. Cytotoxic macrolides from a cultured marine dinoflagellate of the genus Amphidinium. Journal of Natural Products, 52(5): 1036–1041.
Kokou F., Makridis P., Kentouri M. and Divanach P. 2012. Antibacterial activity in microalgae cultures. Aquaculture Research, 43(10): 1520–1527.
LaJeunesse T.C., Lambert G., Andersen R.A., Coffroth M.A. and Galbraith D.W. 2005. Symbiodinium (Pyrrophyta) genome sizes (DNA content) are smallest among dinoflagellates 1. Journal of Phycology, 41(4): 880–886.
Leone A., Lecci R.M., Durante M. and Piraino S. 2013. Extract from the zooxanthellate jellyfish Cotylorhiza tuberculata modulates gap junction intercellular communication in human cell cultures. Marine Drugs, 11(5): 1728–1762.
Leutou A.S., McCall J.R., York R., Govindapur R.R. and Bourdelais A.J. 2020. Anti-inflammatory activity of glycolipids and a polyunsaturated fatty acid methyl ester isolated from the marine dinoflagellate Karenia mikimotoi. Marine Drugs, 18(3): 1–12 (138).
Malik Z., Hanania J. and Nitzan Y. 1990. New trends in photobiology bactericidal effects of photoactivated porphyrins- An alternative approach to antimicrobial drugs. Journal of Photochemistry and Photobiology (B), 5(3-4): 281–293.
McConnaughey T.A. 2012. Zooxanthellae that open calcium channels: Implications for reef corals. Marine Ecology Progress Series, 460: 277–287.
Mclaughlin J.L., Rogers L.L. and Anderson J.E. 1998. The use of biological assays to evaluate botanicals. Drug Information Journal, 32(2): 513–524.
Nabipour I., Najafi A. and Bou A.A. 2009. Anticancer and cytotoxic compounds from seashells of the Persian Gulf. Iranian South Medical Journal 12(3): 231–237.
Nagai H., Satake M. and Yasumoto T. 1990. Antimicrobial activities of polyether compounds of dinoflagellate origins. Journal of Applied Phycology, 2(4): 305–308.
Nakamura H., Asari T., Ohizumi Y., Kobayashi J.I., Yamasu T. and Murai A. 1993. Isolation of zooxanthellatoxins, novel vasoconstrictive substances from the zooxanthella Symbiodinium sp. Toxicon, 31(4): 371–376.
Nakamura H., Kawase Y., Maruyama K. and Murai A. 1998. Studies on polyketide metabolites of a symbiotic dinoflagellate, Symbiodinium sp.: A new C30 marine alkaloid, zooxanthellamine, a plausible precursor for zoanthid alkaloids. Bulletin of the Chemical Society of Japan, 71(4): 781–787.
NCCLS (National Committee for Clinical Laboratory Standards). 1997. Performance standards for anti-microbial disk susceptibility test. Approved Standard. M100-A6. NCCLS, USA. 13P
Onodera K.I., Konishi Y., Taguchi T., Kiyoto S. and Tominaga A. 2014. Peridinin from the marine symbiotic dinoflagellate, Symbiodinium sp., regulates eosinophilia in mice. Marine Drugs, 12(4): 1773–1787.
Onodera K.I., Nakamura H., Oba Y., Ohizumi Y. and Ojika M. 2005. Zooxanthellamide Cs: vasoconstrictive polyhydroxylated macrolides with the largest lactone ring size from a marine dinoflagellate of Symbiodinium sp. Journal of the American Chemical Society, 127(29): 10406–10411.
PolneFuller M. 1991. A novel technique for prpeparation of axenic cultures of Symbiodinium (Pyrrophyta) through selective digestion by amoebae 1. Journal of Phycology, 27(4): 552–554.
Rogers J.E. and Marcovich D. 2007. A simple method for the extraction and quantification of photopigments from Symbiodinium spp. Journal of Experimental Marine Biology and Ecology, 353(2): 191–197.
Samarakoon K.W., Ko J.Y., Rahman S.M., Lee J.H., Kang M.C., Kwon O.N., Lee J.B. and Jeon Y.J. 2013. In vitro studies of anti-inflammatory and anticancer activities of organic solvent extracts from cultured marine microalgae. Algae, 28(1): 111–119.
Schoenberg D.A. and Trench R.K. 1980. Genetic variation in Symbiodinium (= Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proceedings of the Royal Society of London, 207(1169): 405–427.
Senanayake S.N., Ahmed N. and Fichtali J. 2010. Nutraceuticals and Bioactives from Marine Algae. Handbook of Seafood Quality, Safety and Health Applications. Wiley-Blackwell, India. 542P.
Shannon E. and Abu-Ghannam N. 2016. Antibacterial derivatives of marine algae: An overview of pharmacological mechanisms and applications. Marine Drugs, 14(4): 1–23 (81).
Shilpa K., Varun K. and Lakshmi B.S. 2010. An alternate method of natural drug production: Eliciting secondary metabolite production using plant cell culture. Journal of Plant Sciences, 5(3): 222–247.
Sugawara T., Yamashita K., Sakai S., Asai A., Nagao A., Shiraishi T., Imai I. and Hirata T. 2007. Induction of apoptosis in DLD-1 human colon cancer cells by peridinin isolated from the dinoflagellate, Heterocapsa triquetra. Bioscience, Biotechnology and Biochemistry, 71(4): 1069–1072.
Trick C.G., Andersen R.J. and Harrison P.J. 1984. Environmental factors influencing the production of an antibacterial metabolite from a marine dinoflagellate, Prorocentrum minimum. Canadian Journal of Fisheries and Aquatic Sciences, 41(3): 423–432.
Washida K., Koyama T., Yamada K., Kita M. and Uemura D. 2006. Karatungiols A and B, two novel antimicrobial polyol compounds, from the symbiotic marine dinoflagellate Amphidinium sp. Tetrahedron Letters, 47(15): 2521–2525.
Williams G.P., Babu S., Ravikumar S., Kathiresan K., Prathap S.A., Chinnapparaj S., Marian M.P. and Alikhan S.L. 2007. Antimicrobial activity of tissue and associated bacteria from benthic sea anemone Stichodactyla haddoni against microbial pathogens. Journal of Environmental Biology, 28(4): 789–793.
Yousefzadi M., Riahi-Madvar A., Hadian J., Rezaee F., Rafiee R. and Biniaz M. 2014. Toxicity of essential oil of Satureja khuzistanica: In vitro cytotoxicity and anti-microbial activity. Journal of Immunotoxicology, 11(1): 50–55.