Antioxidant of the endosymbiotic dinoflagellate Symbiodinium sp. from the sea anemone Stichodactyla haddoni Saville-Kent
Section:
Physiology, Biochemistry. BiophysicsIssue:
Vol. 35 No. 1 (2025)Pages:
15-29DOI:
https://doi.org/10.15407/alg35.01.015Abstract
Marine dinoflagellates are potentially useful for many biomedical, toxicological and ecological applications. This study focuses on determining the antioxidant properties of Symbiodinium sp. isolated from the sea anemone Stichodactyla haddoni, collected from the Persian Gulf and the Gulf of Oman in 2018 and 2019, purified and cultured also in vitro. Antioxidant activity and total antioxidant activity were determined by two methods using 2,2-diphenyl-1-picrylhydrazyl (DPPH) free radical and ferric-reducing antioxidant power (FRAP). The highest DPPH radical scavenging activity detected was 135.78 μg · mL-1 in the methanolic extract of Symbiodinium sp. from the winter Chabahar Bay sample using LC50. The FRAP method showed the maximum antioxidant activity (0.3 μg mL-1) in the methanolic extract at the concentration of 2 mg · mL-1 in the same sample. Cluster heatmap analysis showed that antioxidant activity was highly correlated with physicochemical factors (temperature and salinity) in the methanolic extract of Symbiodinium sp. Our results showed that the role of antioxidants and the types of ROS that are predominantly neutralized by peridinin and diatoxanthin should be more carefully studied, and we recommend using the electron spin resonance (ESR) spectroscopic method to determine the antioxidant properties of algae that contain these pigments.
Keywords:
zooxanthellae, symbiont, culture, antioxidant, Indian OceanFull text
References
Dang K.V., Pierangelini M., Roberty S., Cardol P. 2019. Alternative photosynthetic electron transfers and bleaching phenotypes upon acute heat stress in Symbiodinium and Breviolum spp. (Symbiodiniaceae) in culture. Front. Mar. Sci. 6: 656. https://doi.org/10.3389/fmars.2019.00656
Davy S.K., Allemand D., Weis V.M. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76(2): 229–261. https://doi.org/10.1128/MMBR.05014-11 https://www.ncbi.nlm.nih.gov/pubmed/22688813 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3372257
Ganesan K., Kumar K.S., Rao P.S. 2011. Comparative assessment of antioxidant activity in three edible species of green seaweed, Enteromorpha from Okha, Northwest coast of India. Innovat. Food Sci. Emerg. Technol. 12(1): 73–78. https://doi.org/10.1016/j.ifset.2010.11.005
Gordon B.R., Leggat W. 2010. Symbiodinium – invertebrate symbioses and the role of metabolomics. Mar. Drugs. 8(10): 2546–2568. https://doi.org/10.3390/md8102546 https://www.ncbi.nlm.nih.gov/pubmed/21116405 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2992991
Gulcin I. 2020. Antioxidants and antioxidant methods: An updated overview. Arch. Toxicol. 94(3): 651–715. https://doi.org/10.1007/s00204-020-02689-3 https://www.ncbi.nlm.nih.gov/pubmed/32180036
Hamanaka R.B., Chandel N.S. 2009. Mitochondrial reactive oxygen species regulate hypoxic signaling. Curr. Opin. Cell Biol. 21(6): 894–899. https://doi.org/10.1016/j.ceb.2009.08.005 https://www.ncbi.nlm.nih.gov/pubmed/19781926 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2787901
Ishikawa C., Jomori T., Tanaka J., Senba M., Mori N. 2016. Peridinin, a carotenoid, inhibits proliferation and survival of HTLV-1-infected T-cell lines. Int. J. Onc. 49(4): 1713–1721. https://doi.org/10.3892/ijo.2016.3648 https://www.ncbi.nlm.nih.gov/pubmed/27499015
Iwasaki H. 1961. The life-cycle of Porphyratenera in vitro. Biol. Bull. 121(1): 173–187. https://doi.org/10.2307/1539469
Jacob-Lopes E., Queiroz M.I., Zepka L.Q. 2020. Pigments from Microalgae Handbook. Switzerland: Springer Nat. 214 p. https://doi.org/10.1007/978-3-030-50971-2
Johansen J.E., Svec W.A., Liaaen-Jensen S., Haxo F.T., 1974. Carotenoids of the Dinophyceae. Phytochemistry. 13(10): 2261–2271. https://doi.org/10.1016/0031-9422(74)85038-7
Krueger T., Becker S., Pontasch S., Dove S., Hoegh‐Guldberg O., Leggat W., Fisher P.L., Davy S.K. 2014. Antioxidant plasticity and thermal sensitivity in four types of Symbiodinium sp. J. Phycol. 50(6): 1035–1047. https://doi.org/10.1111/jpy.12232 https://www.ncbi.nlm.nih.gov/pubmed/26988785
Laskey R.A. 1970. The use of antibiotics in the preparation of amphibian cell cultures from highly contaminated material. J. Cell Sci. 7(3): 653–659. https://doi.org/10.1242/jcs.7.3.653 https://www.ncbi.nlm.nih.gov/pubmed/4321684
Lesser M.P. 2011. Coral bleaching: causes and mechanisms. In: Coral reefs: An ecosystem in transition. Dordrecht: Springer. Pp. 405–419. https://doi.org/10.1007/978-94-007-0114-4_23
Muscatine L.E., Porter J.W. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience. 27(7): 454–460. https://doi.org/10.2307/1297526
Muscatine L., Karakashian S.J., Karakashian M.W. 1967. Soluble extracellular products of algae symbiotic with a ciliate, a sponge and a mutant hydra. Comp. Biochem. Physiol. 20(1): 1–2. https://doi.org/10.1016/0010-406X(67)90720-7
Olpp T., Brückner R. 2006. Total synthesis of the light-harvesting carotenoid peridinin. Angew. Chem. Int. Edit. 45(24): 4023–4027. https://doi.org/10.1002/anie.200600502 https://www.ncbi.nlm.nih.gov/pubmed/16683293
Olson J.A. 1999. Carotenoids and human health. Arch. Latinoam. Nutr. 49(3 Suppl 1): 7S–11S.
Oyaizu M. 1986. Studies on products of browning reaction. Jap. J. Nutr. Diet. 44(6): 307–315. https://doi.org/10.5264/eiyogakuzashi.44.307
Pandolfi J.M., Bradbury R.H., Sala E., Hughes T.P., Bjorndal K.A., Cooke R.G., McArdle D., McClenachan L., Newman M.J., Paredes G., Warner R.R. 2003. Global trajectories of the long-term decline of coral reef ecosystems. Science. 301(5635): 955–958. https://doi.org/10.1126/science.1085706 https://www.ncbi.nlm.nih.gov/pubmed/12920296
Polne-Fuller M. 1991. A novel technique for preparation of axenic cultures of Symbiodinium (Pyrrophyta). J. Phycol. 27(4): 552–554. https://doi.org/10.1111/j.0022-3646.1991.00552.x
Roberty S., Furla P., Plumier J.C. 2016. Differential antioxidant response between two Symbiodinium species from contrasting environments. Plant, Cell Environ. 39(12): 2713–2724. https://doi.org/10.1111/pce.12825 https://www.ncbi.nlm.nih.gov/pubmed/27577027
Roberty S., Fransolet D., Cardol P., Plumier J.C., Franck F. 2015. Imbalance between oxygen photoreduction and antioxidant capacities in Symbiodinium cells exposed to combined heat and high light stress. Coral Reefs. 34(4): 1063–1073. https://doi.org/10.1007/s00338-015-1328-5
Rodriguez R., Redman R. 2005. Balancing the generation and elimination of reactive oxygen species. Proc. Nat. Acad. Sci. 102(9): 3175–3176. https://doi.org/10.1073/pnas.0500367102 https://www.ncbi.nlm.nih.gov/pubmed/15728396 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC552941
Sha M.M.R., Samarakoon K.W., An S., Jeon Y., Lee J. 2016. Growth characteristics of three benthic dinoflagellates in mass culture and their antioxidant properties. J. Fisher. Aquat. Sci. 11: 268–277. https://doi.org/10.3923/jfas.2016.268.277
Trench R.K. 1971a. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. I. The assimilation of photosynthetic products of zooxanthellae by two marine coelenterates. Proc. Roy. Soc. London. Ser. B. 177(1047): 225–235. https://doi.org/10.1098/rspb.1971.0024
Trench R.K. 1971b. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. Liberation of fixed 14C by zooxanthellae in vitro. Proc. Roy. Soc. London. Ser. B. 177(1047): 237–250. https://doi.org/10.1098/rspb.1971.0025
Trench R.K. 1971c. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates III. The effect of homogenates of host tissues on the excretion of photosynthetic products in vitro by zooxanthellae from two marine coelenterates. Proc. Roy. Soc. London. Ser. B. 177(1047): 251–264. https://doi.org/10.1098/rspb.1971.0026
Wakefield T.S., Kempf S.C. 2001. Development of host-and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biol. Bull. 200(2): 127–143. https://doi.org/10.2307/1543306 https://www.ncbi.nlm.nih.gov/pubmed/11341574
Weis V.M. 2008. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211(19): 3059–3066. https://doi.org/10.1242/jeb.009597 https://www.ncbi.nlm.nih.gov/pubmed/18805804
Widowati I., Zainuri M., Kusumaningrum H.P., Susilowati R., Hardivillier Y., Leignel V., Mouget J.L. 2017. Antioxidant activity of three microalgae Dunaliellasalina, Tetraselmischuii and Isochrysisgalbana clone Tahiti. IOP Conf. Ser.: Earth Environ. Sci. 55(1): 01206. https://doi.org/10.1088/1755-1315/55/1/012067
Wietheger A., Fisher P.L., Gould K.S., Davy S.K. 2015. Sensitivity to oxidative stress is not a definite predictor of thermal sensitivity in symbiotic dinoflagellates. Mar. Biol. 162(10): 2067–2077. https://doi.org/10.1007/s00227-015-2736-3
Zahl P.A., McLaughlin J.O. 1957. Isolation and cultivation of zooxanthellae. Nature. 180(4578): 199–200. https://doi.org/10.1038/180199a0