ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Semi-continuous cultivation of the mixotrophic dinoflagellate Gymnodinium smaydae, a new promising microalga for omega-3 production

  • Lim, An Suk (Division of Life Science & Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • You, Ji Hyun (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Park, Sang Ah (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2020.07.25
  • Accepted : 2020.09.02
  • Published : 2020.09.21
Download PDF
⟨ Previous Next ⟩

Abstract

Omega-3 fatty acids, including eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), are polyunsaturated fatty acids beneficial to human health. A limited number of microalgae have been used for commercial omega-3 production, which necessitates the identification of new microalgae with high omega-3 contents. We explored the fatty acid composition and EPA and DHA contents of the mixotrophic dinoflagellate Gymnodinium smaydae fed with the optimal algal prey species Heterocapsa rotundata. Cells of G. smaydae were found to be rich in omega-3 fatty acids. In particular, the DHA content of G. smaydae was 21 mg g-1 dry weight, accounting for 43% of the total fatty acid content. The percentage of DHA in the total fatty acid content of G. smaydae was the highest among the reported microalgae except for Crypthecodinium cohnii. Moreover, to determine if the prey supply interval affected the growth rate of G. smaydae and its fatty acid content, three different prey supply intervals (daily, once every 2 d, and once for 4 d) were tested. Daily prey supply yielded the highest total fatty acid and DHA contents in G. smaydae. Furthermore, we successfully produced high-density G. smaydae cultures semi-continuously for 43 d with daily prey supply. During the semi-continuous cultivation period, the highest density of G. smaydae was 57,000 cells mL-1, with an average growth rate of 0.7 d-1. Taken together, the percentage of EPA and DHA in the total fatty acid content was maintained in the range of 54.2-56.9%. The results of this study support G. smaydae as a promising microalgal candidate for commercial DHA production and demonstrate that daily supply of prey can efficiently produce high-density G. smaydae cultures for more than a month.

Keywords

References

  1. Adolf, J. E., Place, A. R., Stoecker, D. K. & Harding, L. W. Jr. 2007. Modulation of polyunsaturated fatty acids in mixotrophic Karlodinium veneficum (Dinophyceae) and its prey, Storeatula major (Cryptophyceae). J. Phycol. 43:1259-1270. https://doi.org/10.1111/j.1529-8817.2007.00419.x
  2. Assuncao, J., Guedes, A. C. & Malcata, F. X. 2017. Biotechnological and pharmacological applications of biotoxins and other bioactive molecules from dinoflagellates. Mar. Drugs 15:393. https://doi.org/10.3390/md15120393
  3. Benstein, R. M., Cebi, Z., Podola, B. & Melkonian, M. 2014. Immobilized growth of the peridinin-producing marine dinoflagellate Symbiodinium in a simple biofilm photobioreactor. Mar. Biotechnol. 16:621-628. https://doi.org/10.1007/s10126-014-9581-0
  4. Berthold, D. E., de la Rosa, N., Engene, N., Jayachandran, K., Gantar, M., Laughinghouse, H. D. & Shetty, K. G. 2020. Omega-7 producing alkaliphilic diatom Fistulifera sp. (Bacillariophyceae) from Lake Okeechobee, Florida. Algae 35:91-106. https://doi.org/10.4490/algae.2020.35.12.16
  5. Blossom, H. E., Daugbjerg, N. & Hansen, P. J. 2012. Toxic mucus traps: a novel mechanism that mediates prey uptake in the mixotrophic dinoflagellate Alexandrium pseudogonyaulax. Harmful Algae 17:40-53. https://doi.org/10.1016/j.hal.2012.02.010
  6. Camacho, F. G., Rodriguez, J. G., Miron, A. S., Garcia, M. C. C., Belarbi, E. H., Chisti, Y. & Grima, E. M. 2007. Biotechnological significance of toxic marine dinoflagellates. Biotechnol. Adv. 25:176-194. https://doi.org/10.1016/j.biotechadv.2006.11.008
  7. Cheirsilp, B. & Torpee, S. 2012. Enhanced growth and lipid production of microalgae under mixotrophic culture condition: effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour. Technol. 110:510-516. https://doi.org/10.1016/j.biortech.2012.01.125
  8. Chua, E. T. & Schenk, P. M. 2017. A biorefinery for Nannochloropsis induction, harvesting, and extraction of EPA-rich oil and high-value protein. Bioresour. Technol. 244:1416-1424. https://doi.org/10.1016/j.biortech.2017.05.124
  9. Cuellar-Bermudez, S. P., Aguilar-Hernandez, I., Cardenas-Chavez, D. L., Ornelas-Soto, N., Romero-Ogawa, M. A. & Parra-Saldivar, R. 2015. Extraction and purification of high-value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microb. Biotechnol. 8:190-209. https://doi.org/10.1111/1751-7915.12167
  10. De Swaaf, M. E., Sijtsma, L. & Pronk, J. T. 2003. High-celldensity fed-batch cultivation of the docosahexaenoic acid producing marine alga Crypthecodinium cohnii. Biotechnol. Bioeng. 81:666-672. https://doi.org/10.1002/bit.10513
  11. Dhanya, B. S., Sowmiya, G., Jeslin, J., Chamundeeswari, M. & Verma, M. L. 2020. Algal biotechnology: a sustainable route for omega-3 fatty acid production. In Alam M. A., Xu, J. -L. & Wang, Z. (Eds.) Microalgae Biotechnology for Food, Health and High Value Products. Springer, Singapore, pp. 125-145.
  12. Doughman, S. D., Krupanidhi, S. & Sanjeevi, C. B. 2007. Omega-3 fatty acids for nutrition and medicine: considering microalgae oil as a vegetarian source of EPA and DHA. Curr. Diabetes Rev. 3:198-203. https://doi.org/10.2174/157339907781368968
  13. Dunstan, G. A., Volkman, J. K., Jeffrey, S. W. & Barrett, S. M. 1992. Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 2. Lipid classes and fatty acids. J. Exp. Mar. Biol. Ecol. 161:115-134. https://doi.org/10.1016/0022-0981(92)90193-E
  14. Ethier, S., Woisard, K., Vaughan, D. & Wen, Z. 2011. Continuous culture of the microalgae Schizochytrium limacinum on biodiesel-derived crude glycerol for producing docosahexaenoic acid. Bioresour. Technol. 102:88-93. https://doi.org/10.1016/j.biortech.2010.05.021
  15. Fajardo, A. R., Cerdan, L. E., Medina, A. R., Fernandez, F. G. A., Moreno, P. A. G. & Grima, E. M. 2007. Lipid extraction from the microalga Phaeodactylum tricornutum. Eur. J. Lipid Sci. Technol. 109:120-126. https://doi.org/10.1002/ejlt.200600216
  16. Fan, K. -W., Jiang, Y., Faan, Y. -W. & Chen, F. 2007. Lipid characterization of mangrove thraustochytrid-Schizochytrium mangrovei. J. Agric. Food Chem. 55:2906-2910. https://doi.org/10.1021/jf070058y
  17. Fuentes-Grunewald, C., Bayliss, C., Fonlut, F. & Chapuli, E. 2016. Long-term dinoflagellate culture performance in a commercial photobioreactor: Amphidinium carterae case. Bioresour. Technol. 218:533-540. https://doi.org/10.1016/j.biortech.2016.06.128
  18. Gallardo-Rodriguez, J. J., Garcia, M. D. C. C., Camacho, F. G., Miron, A. S., Belarbi, E. H. & Grima, E. M. 2007. New culture approaches for yessotoxin production from the dinoflagellate Protoceratium reticulatum. Biotechnol. Prog. 23:339-350. https://doi.org/10.1021/bp060221u
  19. Gallardo-Rodriguez, J. J. G., Miron, A. S., Camacho, F. G., Garcia, M. C. C., Belarbi, E. H. & Grima, E. M. 2010. Culture of dinoflagellates in a fed-batch and continuous stirredtank photobioreactors: growth, oxidative stress and toxin production. Process Biochem. 45:660-666. https://doi.org/10.1016/j.procbio.2009.12.018
  20. Gallardo-Rodriguez, J., Sanchez-Miron, A., Garcia-Camacho, F., Lopez-Rosales, L., Chisti, Y. & Molina-Grima, E. 2012. Bioactives from microalgal dinoflagellates. Biotechnol. Adv. 30:1673-1684. https://doi.org/10.1016/j.biotechadv.2012.07.005
  21. Garces, R. & Mancha, M. 1993. One-step lipid extraction and fatty acid methyl esters preparation from fresh plant tissues. Anal. Biochem. 211:139-143. https://doi.org/10.1006/abio.1993.1244
  22. Gunstone, F. D. 1996. Fatty acid and lipid chemistry. Blackie Academic, London, 263 pp.
  23. Gupta, A., Barrow, C. J. & Puri, M. 2012. Omega-3 biotechnology: thraustochytrids as a novel source of omega-3 oils. Biotechnol. Adv. 30:1733-1745. https://doi.org/10.1016/j.biotechadv.2012.02.014
  24. Holmes, M. J., Brust, A. & Lewis, R. J. 2014. Dinoflagellate toxins: an overview. In Botana, L. M. (Ed.) Seafood and Freshwater Toxins: Pharmacology, Physiology, and Detection. 3rd ed. CRC Press, Boca Raton, FL, pp. 3-38.
  25. Horrocks, L. A. & Yeo, Y. K. 1999. Health benefits of docosahexaenoic acid (DHA). Pharmacol. Res. 40:211-225. https://doi.org/10.1006/phrs.1999.0495
  26. Jang, S. H., Jeong, H. J. & Kwon, J. E. 2017. High contents of eicosapentaenoic acid and docosahexaenoic acid in the mixotrophic dinoflagellate Paragymnodinium shiwhaense and identification of putative omega-3 biosynthetic genes. Algal Res. 25:525-537. https://doi.org/10.1016/j.algal.2017.06.020
  27. Jeong, H. J. & Lim, A. S. 2020. Method and system for continuous mass culture for mixotrophic dinoflagellates. Patent no. KR102064718B1. Korean Intellectual Property Office, Daejeon.
  28. Jeong, H. J., Lim, A. S., Franks, P. J. S., Lee, K. H., Kim, J. H., Kang, N. S., Lee, M. J., Jang, S. H., Lee, S. Y., Yoon, E. Y., Park, J. Y., Yoo, Y. D., Seong, K. A., Kwon, J. E. & Jang, T. Y. 2015. A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97-115. https://doi.org/10.1016/j.hal.2015.06.004
  29. Jeong, H. J., Lim, A. S., Lee, K., Lee, M. J., Seong, K. A., Kang, N. S., Jang, S. H., Lee, K. H., Lee, S. Y., Kim, M. O., Kim, J. H., Kwon, J. E., Kang, H. C., Kim, J. S., Yih, W., Shin, K., Jang, P. K., Ryu, J. -H., Kim, S. Y., Park, J. Y. & Kim, K. Y. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. Temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae 32:101-130. https://doi.org/10.4490/algae.2017.32.5.30
  30. Jeong, H. J., Yoo, Y. D., Kang, N. S., Lim, A. S., Seong, K. A., Lee, S. Y., Lee, M. J., Lee, K. H., Kim, H. S., Shin, W., Nam, S. W., Yih, W. & Lee, K. 2012. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl. Acad. Sci. U. S. A. 109:12604-12609. https://doi.org/10.1073/pnas.1204302109
  31. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S. & Kim, T. H. 2010. Growth, feeding, and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45:65-91. https://doi.org/10.1007/s12601-010-0007-2
  32. Jeong, H. J., Yoo, Y. D., Lee, K. H., Kim, T. H., Seong, K. A., Kang, N. S., Lee, S. Y., Kim, J. S., Kim, S. & Yih, W. H. 2013. Red tides in Masan Bay, Korea in 2004-2005: I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae 30S(Suppl. 1):S75-S88.
  33. Jiang, Y. & Chen, F. 2000. Effects of temperature and temperature shift on docosahexaenoic acid production by the marine microalge Crypthecodinium cohnii. J. Am. Oil Chem. Soc. 77:613-617. https://doi.org/10.1007/s11746-000-0099-0
  34. Jiang, Y., Chen, F. & Liang, S. -Z. 1999. Production potential of docosahexaenoic acid by the heterotrophic marine dinoflagellate Crypthecodinium cohnii. Process Biochem. 34:633-637. https://doi.org/10.1016/S0032-9592(98)00134-4
  35. Jiang, Y., Fan, K. -W., Tsz-Yeung Wong, R. & Chen, F. 2004. Fatty acid composition and squalene content of the marine microalga Schizochytrium mangrovei. J. Agric. Food Chem. 52:1196-1200. https://doi.org/10.1021/jf035004c
  36. Kang, H. C., Jeong, H. J., Ok, J. H., You, J. H., Jang, S. H., Lee, S. Y., Lee, K. H., Park, J. Y. & Rho, J. -R. 2019. Spatial and seasonal distributions of the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) in Korea: quantification using qPCR. Algae 34:111-126. https://doi.org/10.4490/algae.2019.34.5.25
  37. Kang, N. S., Jeong, H. J., Moestrup, O., Lee, S. Y., Lim, A. S., Jang, T. Y., Lee, K. H., Lee, M. J., Jang, S. H., Potvin, E., Lee, S. K. & Noh, J. H. 2014. Gymnodinium smaydae n. sp., a new planktonic phototrophic dinoflagellate from the coastal waters of western Korea: morphology and molecular characterization. J. Eukaryot. Microbiol. 61:182-203. https://doi.org/10.1111/jeu.12098
  38. Kang, N. S., Kim, E. S., Lee, J. A., Kim, K. M., Kwak, M. S., Yoon, M. & Hong, J. W. 2020. First report of the dinoflagellate genus Effrenium in the east sea of Korea: morphological, genetic, and fatty acid characteristics. Sustainability 12:3928. https://doi.org/10.3390/su12093928
  39. Khan, M. I., Shin, J. H. & Kim, J. D. 2018. The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb. Cell Fact. 17:36. https://doi.org/10.1186/s12934-018-0879-x
  40. Kim, S., Kang, Y. G., Kim, H. S., Yih, W., Coats, D. W. & Park, M. G. 2008. Growth and grazing responses of the mixotrophic dinoflagellate Dinophysis acuminata as functions of light intensity and prey concentration. Aquat. Microb. Ecol. 51:301-310. https://doi.org/10.3354/ame01203
  41. LaJeunesse, T. C., Parkinson, J. E., Gabrielson, P. W., Jeong, H. J., Reimer, J. D., Voolstra, C. R. & Santos, S. R. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28:2570-2580. https://doi.org/10.1016/j.cub.2018.07.008
  42. Lee, B. I., Kim, S. K., Kim, J. H., Kim, H. S., Kim, J. I., Shin, W., Rho, J. -R. & Yih, W. 2019a. Intraspecific variations in macronutrient, amino acid, and fatty acid composition of mass-cultured Teleaulax amphioxeia (Cryptophyceae) strains. Algae 34:163-175. https://doi.org/10.4490/algae.2019.34.6.4
  43. Lee, K. H., Jeong, H. J., Jang, T. Y., Lim, A. S., Kang, N. S., Kim, J. -H., Kim, K. Y., Park, K. -T. & Lee, K. 2014. Feeding by the newly described mixotrophic dinoflagellate Gymnodinium smaydae: feeding mechanism, prey species, and effect of prey concentration. J. Exp. Mar. Biol. Ecol. 459:114-125. https://doi.org/10.1016/j.jembe.2014.05.011
  44. Lee, K. H., Jeong, H. J., Kang, H. C., Ok, J. H., You, J. H. & Park, S. A. 2019b. Growth rates and nitrate uptake of co-occurring red-tide dinoflagellates Alexandrium affine and A. fraterculus as a function of nitrate concentration under light-dark and continuous light conditions. Algae 34:237-251. https://doi.org/10.4490/algae.2019.34.8.28
  45. Leu, S. & Boussiba, S. 2014. Advances in the production of high-value products by microalgae. Ind. Biotechnol. 10:169-183. https://doi.org/10.1089/ind.2013.0039
  46. Li, A., Stoecker, D. K. & Adolf, J. E. 1999. Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat. Microb. Ecol. 19:163-176. https://doi.org/10.3354/ame019163
  47. Li, X., Xu, H. & Wu, Q. 2007. Large-scale biodiesel production from microalga Chlorella protothecoides through heterotrophic cultivation in bioreactors. Biotechnol. Bioeng. 98:764-771. https://doi.org/10.1002/bit.21489
  48. Liang, Y., Sarkany, N., Cui, Y., Yesuf, J., Trushenski, J. & Blackburn, J. W. 2010. Use of sweet sorghum juice for lipid production by Schizochytrium limacinum SR21. Bioresour. Technol. 101:3623-3627. https://doi.org/10.1016/j.biortech.2009.12.087
  49. Lim, A. S., Jeong, H. J., Kim, S. J. & Ok, J. H. 2018. Amino acids profiles of six dinoflagellate species belonging to diverse families: possible use as animal feeds in aquaculture. Algae 33:279-290. https://doi.org/10.4490/algae.2018.33.9.10
  50. Lim, A. S., Jeong, H. J. & Ok, J. H. 2019a. Five Alexandrium species lacking mixotrophic ability. Algae 34:289-301. https://doi.org/10.4490/algae.2019.34.11.21
  51. Lim, A. S., Jeong, H. J., Ok, J. H., You, J. H., Kang, H. C. & Kim, S. J. 2019b. Effects of light intensity and temperature on growth and ingestion rates of the mixotrophic dinoflagellate Alexandrium pohangense. Mar. Biol. 166:98. https://doi.org/10.1007/s00227-019-3546-9
  52. Mansour, M. P., Frampton, D. M. F., Nichols, P. D., Volkman, J. K. & Blackburn, S. I. 2005. Lipid and fatty acid yield of nine stationary-phase microalgae: applications and unusual $C_{24}-C_{28}$ polyunsaturated fatty acids. J. Appl. Phycol. 17:287-300. https://doi.org/10.1007/s10811-005-6625-x
  53. Martins, D. A., Custodio, L., Barreira, L., Pereira, H., Ben-Hamadou, R., Varela, J. & Abu-Salah, K. M. 2013. Alternative sources of n-3 long-chain polyunsaturated fatty acids in marine microalgae. Mar. Drugs 11:2259-2281. https://doi.org/10.3390/md11072259
  54. Mendes, A., Reis, A., Vasconcelos, R., Guerra, P. & da Silva, T. L. 2009. Crypthecodinium cohnii with emphasis on DHA production: a review. J. Appl. Phycol. 21:199-214. https://doi.org/10.1007/s10811-008-9351-3
  55. Mobin, S. & Alam, F. 2017. Some promising microalgal species for commercial applications: a review. Energy Procedia 110:510-517. https://doi.org/10.1016/j.egypro.2017.03.177
  56. Ning, Y. & Liu, X. 2020. Enteromorpha hydrolysate as carbon source for fatty acids production of microalgae Schizochytrium sp. Energy 203:117900. https://doi.org/10.1016/j.energy.2020.117900
  57. Onodera, K., Konishi, Y., Taguchi, T., Kiyoto, S. & Tominaga, A. 2014. Peridinin from the marine symbiotic dinoflagellate, Symbiodinium sp., regulates eosinophilia in mice. Mar. Drugs 12:1773-1787. https://doi.org/10.3390/md12041773
  58. Paliwal, C., Mitra, M., Bhayani, K., Bharadwaj, S. V. V., Ghosh, T., Dubey, S. & Mishra, S. 2017. Abiotic stresses as tools for metabolites in microalgae. Bioresour. Technol. 244:1216-1226. https://doi.org/10.1016/j.biortech.2017.05.058
  59. Park, W. -K., Moon, M., Shin, S. -E., Cho, J. M., Suh, W. I., Chang, Y. K. & Lee, B. 2018. Economical DHA (docosahexaenoic acid) production from Aurantiochytrium sp. KRS101 using orange peel extract and low cost nitrogen sources. Algal Res. 29:71-79. https://doi.org/10.1016/j.algal.2017.11.017
  60. Patil, V., Kallqvist, T., Olsen, E., Vogt, G. & Gislerod, H. R. 2007. Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquac. Int. 15:1-9. https://doi.org/10.1007/s10499-006-9060-3
  61. Pleissner, D. & Eriksen, N. T. 2012. Effects of phosphorous, nitrogen, and carbon limitation on biomass composition in batch and continuous flow cultures of the heterotrophic dinoflagellate Crypthecodinium cohnii. Biotechnol. Bioeng. 109:2005-2016. https://doi.org/10.1002/bit.24470
  62. Rawat, I., Kumar, R. R., Mutanda, T. & Bux, F. 2013. Biodiesel from microalgae: a critical evaluation from laboratory to large scale production. Appl. Energy 103:444-467. https://doi.org/10.1016/j.apenergy.2012.10.004
  63. Shimizu, Y. 1996. Microalgal metabolites: a new perspective. Annu. Rev. Microbiol. 50:431-465. https://doi.org/10.1146/annurev.micro.50.1.431
  64. Stoecker, D. K., Hansen, P. J., Caron, D. A. & Mitra, A. 2017. Mixotrophy in the marine plankton. Ann. Rev. Mar. Sci. 9:311-335. https://doi.org/10.1146/annurev-marine-010816-060617
  65. Tan, C. H., Show, P. L., Chang, J. -S., Ling, T. C. & Lan, J. C. -W. 2015. Novel approaches of producing bioenergies from microalgae: a recent review. Biotechnol. Adv. 33:1219-1227. https://doi.org/10.1016/j.biotechadv.2015.02.013
  66. Tang, E. P. Y. 1996. Why do dinoflagellates have lower growth rates? J. Phycol. 32:80-84. https://doi.org/10.1111/j.0022-3646.1996.00080.x
  67. Taylor, F. J. R., Hoppenrath, M. & Saldarriaga, J. F. 2008. Dinoflagellate diversity and distribution. Biodivers. Conserv. 17:407-418. https://doi.org/10.1007/s10531-007-9258-3
  68. Thomas, W. H. & Gibson, C. H. 1990. Effects of small-scale turbulence on microalgae. J. Appl. Phycol. 2:71-77. https://doi.org/10.1007/BF02179771
  69. Thompson, P. A., Guo, M. -X., Harrison, P. J. & Whyte, J. N. C. 1992. Effects of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. J. Phycol. 28:488-497. https://doi.org/10.1111/j.0022-3646.1992.00488.x
  70. Torres-Tiji, Y., Fields, F. J. & Mayfield, S. P. 2020. Microalgae as a future food source. Biotechnol. Adv. 41:107536. https://doi.org/10.1016/j.biotechadv.2020.107536
  71. Volkman, J. K., Jeffrey, S. W., Nichols, P. D., Rogers, G. I. & Garland, C. D. 1989. Fatty acid and lipid composition of 10 species of microalgae used in mariculture. J. Exp. Mar. Biol. Ecol. 128:219-240. https://doi.org/10.1016/0022-0981(89)90029-4
  72. Wang, S., Chen, J., Li, Z., Wang, Y., Fu, B., Han, X. & Zheng, L. 2015. Cultivation of the benthic microalga Prorocentrum lima for the production of diarrhetic shellfish poisoning toxins in a vertical flat photobioreactor. Bioresour. Technol. 179:243-248. https://doi.org/10.1016/j.biortech.2014.12.019
  73. Yongmanitchai, W. & Ward, O. P. 1991. Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions. Appl. Environ. Microbiol. 57:419-425. https://doi.org/10.1128/AEM.57.2.419-425.1991
  74. Yoo, Y. D., Jeong, H. J., Kim, M. S., Kang, N. S., Song, J. Y., Shin, W., Kim, K. Y. & Lee, K. 2009. Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 56:413-420. https://doi.org/10.1111/j.1550-7408.2009.00421.x
  75. You, J. H., Jeong, H. J., Lim, A. S., Ok, J. H. & Kang, H. C. 2020. Effects of irradiance and temperature on the growth and feeding of the obligate mixotrophic dinoflagellate Gymnodinium smaydae. Mar. Biol. 167:64. https://doi.org/10.1007/s00227-020-3678-y

Cited by

  1. Antibacterial Activity and Amphidinol Profiling of the Marine Dinoflagellate Amphidinium carterae (Subclade III) vol.22, pp.22, 2020, https://doi.org/10.3390/ijms222212196