ALGAE

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

DOI QR Code

The exceptionally large genome of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae): determination by flow cytometry

  • Hong, Hyun-Hee (School of Biological Sciences and Technology, Chonnam National University) ;
  • Lee, Hyun-Gwan (Department of Oceanography, Chonnam National University) ;
  • Jo, Jihoon (School of Biological Sciences and Technology, Chonnam National University) ;
  • Kim, Hye Mi (Department of Oceanography, Chonnam National University) ;
  • Kim, Su-Man (School of Biological Sciences and Technology, Chonnam National University) ;
  • Park, Jae Yeon (CO2 Recycling Research Center, Advanced Institutes of Convergence Technology, Seoul National University) ;
  • Jeon, Chang Bum (Department of Oceanography, Chonnam National University) ;
  • Kang, Hyung-Sik (School of Biological Sciences and Technology, Chonnam National University) ;
  • Park, Myung Gil (Department of Oceanography, Chonnam National University) ;
  • Park, Chungoo (School of Biological Sciences and Technology, Chonnam National University) ;
  • Kim, Kwang Young (Department of Oceanography, Chonnam National University)
  • Received : 2016.10.22
  • Accepted : 2016.12.06
  • Published : 2016.12.15
Download PDF
⟨ Previous Next ⟩

Abstract

Cochlodinium polykrikoides is a red-tide forming dinoflagellate that causes significant worldwide impacts on aquaculture industries and the marine ecosystem. There have been extensive studies on managing and preventing C. polykrikoides blooms, but it has been difficult to identify an effective method to control the bloom development. There is also limited genome information on the molecular mechanisms involved in its various ecophysiology and metabolism processes. Thus, comprehensive genome information is required to better understand harmful algal blooms caused by C. polykrikoides. We estimated the C. polykrikoides genome size using flow cytometry, with detection of the fluorescence of DNA stained with propidium iodide (PI). The nuclear genome size of C. polykrikoides was 100.97 Gb, as calculated by comparing its mean fluorescence intensity (MFI) to the MFI of Mus musculus, which is 2.8 Gb. The exceptionally large genome size of C. polykrikoides might indicate its complex physiological and metabolic characteristics. Our optimized protocol for estimating the nuclear genome size of a dinoflagellate using flow cytometry with PI can be applied in studies of other marine organisms.

Keywords

References

  1. Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. 2012. Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Ann. Rev. Mar. Sci. 4:143-176. https://doi.org/10.1146/annurev-marine-120308-081121
  2. Beaulieu, J. M., Leitch, I. J., Patel, S., Pendharkar, A. & Knight, C. A. 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytol. 179:975-986. https://doi.org/10.1111/j.1469-8137.2008.02528.x
  3. Cavalier-Smith, T. 2005. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann. Bot. 95:147-175. https://doi.org/10.1093/aob/mci010
  4. Curtiss, C. C., Langlois, G. W., Busse, L. B., Mazzillo, F. & Silver, M. W. 2008. The emergence of Cochlodinium along the California Coast (USA). Harmful Algae 7:337-346. https://doi.org/10.1016/j.hal.2007.12.012
  5. Dolezel, J., Bartos, J., Voglmayr, H. & Greilhuber, J. 2003. Nuclear DNA content and genome size of trout and human. Cytometry A 51:127-128.
  6. Dorantes-Aranda, J. J., Garcia-de la Parra, L. M., Alonso-Rodriguez, R., Morquecho, L. & Voltolina, D. 2010. Toxic effect of the harmful dinoflagellate Cochlodinium polykrikoides on the spotted rose snapper Lutjanus guttatus. Environ. Toxicol. 25:319-326.
  7. Ebenezer, V. & Ki, J.-S. 2014. Biocide sodium hypochlorite decreases pigment production and induces oxidative damage in the harmful dinoflagellate Cochlodinium polykrikoides. Algae 29:311-319. https://doi.org/10.4490/algae.2014.29.4.311
  8. Elliott, T. A. & Gregory, T. R. 2015. What's in a genome? The C-value enigma and the evolution of eukaryotic genome content. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370:20140331. https://doi.org/10.1098/rstb.2014.0331
  9. Garate-Lizarraga, I. 2013. Bloom of Cochlodinium polykrikoides (Dinophyceae: Gymnodiniales) in Bahia de La Paz, Gulf of California. Mar. Pollut. Bull. 67:217-222. https://doi.org/10.1016/j.marpolbul.2012.11.031
  10. Gobler, C. J., Berry, D. L., Anderson, O. R., Burson, A., Koch, F., Rodgers, B. S., Moore, L. K., Goleski, J. A., Allam, B., Bowser, P., Tang, Y. & Nuzzi, R. 2008. Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA. Harmful Algae 7:293-307. https://doi.org/10.1016/j.hal.2007.12.006
  11. Gregory, S. G., Sekhon, M., Schein, J., Zhao, S., Osoegawa, K., Scott, C. E., Evans, R. S., Burridge, P. W., Cox, T. V., Fox, C. A., Hutton, R. D., Mullenger, I. R., Phillips, K. J., Smith, J., Stalker, J., Threadgold, G. J., Birney, E., Wylie, K., Chinwalla, A., Wallis, J., Hillier, L., Carter, J., Gaige, T., Jaeger, S., Kremitzki, C., Layman, D., Maas, J., McGrane, R., Mead, K., Walker, R., Jones, S., Smith, M., Asano, J., Bosdet, I., Chan, S., Chittaranjan, S., Chiu, R., Fjell, C., Fuhrmann, D., Girn, N., Gray, C., Guin, R., Hsiao, L., Krzywinski, M., Kutsche, R., Lee, S. S., Mathewson, C., McLeavy, C., Messervier, S., Ness, S., Pandoh, P., Prabhu, A.-L., Saeedi, P., Smailus, D., Spence, L., Stott, J., Taylor, S., Terpstra, W., Tsai, M., Vardy, J., Wye, N., Yang, G., Shatsman, S., Ayodeji, B., Geer, K., Tsegaye, G., Shvartsbeyn, A., Gebregeorgis, E., Krol, M., Russell, D., Overton, L., Malek, J. A., Holmes, M., Heaney, M., Shetty, J., Feldblyum, T., Nierman, W. C., Catanese, J. J., Hubbard, T., Waterston, R. H., Rogers, J., de Jong, P. J., Fraser, C. M., Marra, M., McPherson, J. D. & Bentley, D. R. 2002. A physical map of the mouse genome. Nature 418:743-750. https://doi.org/10.1038/nature00957
  12. Gregory, T. R. 2001. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. Camb. Philos. Soc. 76:65-101. https://doi.org/10.1017/S1464793100005595
  13. Gregory, T. R. 2002. A bird's-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class aves. Evolution 56:121-130. https://doi.org/10.1111/j.0014-3820.2002.tb00854.x
  14. Gregory, T. R., Nicol, J. A., Tamm, H., Kullman, B., Kullman, K., Leitch, I. J., Murray, B. G., Kapraun, D. F., Greilhuber, J. & Bennett, M. D. 2007. Eukaryotic genome size databases. Nucleic Acids Res 35(Suppl. 1):D332-D338. https://doi.org/10.1093/nar/gkl828
  15. Gregory, T. R. & Witt, J. D. S. 2008. Population size and genome size in fishes: a closer look. Genome 51:309-313. https://doi.org/10.1139/G08-003
  16. Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8:229-239. https://doi.org/10.1139/m62-029
  17. Guo, R., Wang, H., Suh, Y. S. & Ki, J.-S. 2016. Transcriptomic profiles reveal the genome-wide responses of the harmful dinoflagellate Cochlodinium polykrikoides when exposed to the algicide copper sulfate. BMC Genomics 17:29. https://doi.org/10.1186/s12864-015-2341-3
  18. Hare, E. E. & Johnston, J. S. 2011. Genome size determination using flow cytometry of propidium iodide-stained nuclei. In Hare, E. E. & Johnston, J. S. (Eds.) Molecular Methods for Evolutionary Genetics. Vol. 772. Humana Press, NY, pp. 3-12.
  19. Kang, E. J., Kim, J.-H., Kim, K., Choi, H.-G. & Kim, K. Y. 2014. Re-evaluation of green tide-forming species in the Yellow Sea. Algae 29:267-277. https://doi.org/10.4490/algae.2014.29.4.267
  20. LaJeunesse, T. C., Lambert, G., Andersen, R. A., Coffroth, M. A. & Galbraith, D. W. 2005. Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J. Phycol. 41:880-886. https://doi.org/10.1111/j.0022-3646.2005.04231.x
  21. Lin, S. 2011. Genomic understanding of dinoflagellates. Res. Microbiol. 162:551-569. https://doi.org/10.1016/j.resmic.2011.04.006
  22. Lin, S., Cheng, S., Song, B., Zhong, X., Lin, X., Li, W., Li, L., Zhang, Y., Zhang, H., Ji, Z., Cai, M., Zhuang, Y., Shi, X., Lin, L., Wang, L., Wang, Z., Liu, X., Yu, S., Zeng, P., Hao, H., Zou, Q., Chen, C., Li, Y., Wang, Y., Xu, C., Meng, S., Xu, X., Wang, J., Yang, H., Campbell, D. A., Sturm, N. R., Dagenais-Bellefeuille, S. & Morse, D. 2015. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350:691-694. https://doi.org/10.1126/science.aad0408
  23. Lynch, M. & Conery, J. S. 2003. The origins of genome complexity. Science 302:1401-1404. https://doi.org/10.1126/science.1089370
  24. Richlen, M. L., Morton, S. L., Jamali, E. A., Rajan, A. & Anderson, D. M. 2010. The catastrophic 2008-2009 red tide in the Arabian gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides. Harmful Algae 9:163-172. https://doi.org/10.1016/j.hal.2009.08.013
  25. Shoguchi, E., Shinzato, C., Kawashima, T., Gyoja, F., Mungpakdee, S., Koyanagi, R., Takeuchi, T., Hisata, K., Tanaka, M., Fujiwara, M., Hamada, M., Seidi, A., Fujie, M., Usami, T., Goto, H., Yamasaki, S., Arakaki, N., Suzuki, Y., Sugano, S., Toyoda, A., Kuroki, Y., Fujiyama, A., Medina, M., Coffroth, M. A., Bhattacharya, D. & Satoh, N. 2013. Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr. Biol. 23:1399-1408. https://doi.org/10.1016/j.cub.2013.05.062
  26. Thornhill, D. J., Lajeunesse, T. C. & Santos, S. R. 2007. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol. Ecol. 16:5326-5340. https://doi.org/10.1111/j.1365-294X.2007.03576.x
  27. Veldhuis, M. J. W., Cucci, T. L. & Sieracki, M. E. 1997. Cellular DNA content of marine phytoplankton using two new fluorochromes: taxonomic and ecological implications. J. Phycol. 33:527-541. https://doi.org/10.1111/j.0022-3646.1997.00527.x
  28. Vinogradov, A. E. 2004. Evolution of genome size: multilevel selection, mutation bias or dynamical chaos? Curr. Opin. Genet. Dev. 14:620-626. https://doi.org/10.1016/j.gde.2004.09.007
  29. Wisecaver, J. H. & Hackett, J. D. 2011. Dinoflagellate genome evolution. Annu. Rev. Microbiol. 65:369-387. https://doi.org/10.1146/annurev-micro-090110-102841
  30. Wolny, J. L., Scott, P. S., Tustison, J. & Brooks, C. R. 2015. Monitoring the 2007 Florida east coast Karenia brevis (Dinophyceae) red tide and neurotoxic shellfish poisoning (NSP) event. Algae 30:49-58. https://doi.org/10.4490/algae.2015.30.1.049
  31. Zingone, A. & Enevoldsen, H. O. 2000. The diversity of harmful algal blooms: a challenge for science and management. Ocean Coast. Manage. 43:725-748. https://doi.org/10.1016/S0964-5691(00)00056-9

Cited by

  1. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: II. Heterotrophic protists and their grazing impacts on red-tide organisms vol.32, pp.3, 2017, https://doi.org/10.4490/algae.2017.32.8.25
  2. An advanced tool, droplet digital PCR (ddPCR), for absolute quantification of the red-tide dinoflagellate, Cochlodinium polykrikoides Margalef (Dinophyceae) vol.32, pp.3, 2017, https://doi.org/10.4490/algae.2017.32.9.10
  3. and Common Heterotrophic Protists vol.65, pp.5, 2018, https://doi.org/10.1111/jeu.12506
  4. Flow Cytometry as a Method to Study Marine Unicellular Algae: Development, Problems, and Prospects vol.45, pp.5, 2016, https://doi.org/10.1134/s1063074019050079
  5. Rapid succession drives spring community dynamics of small protists at Helgoland Roads, North Sea vol.42, pp.3, 2016, https://doi.org/10.1093/plankt/fbaa017
  6. Dependence of genome size and copy number of rRNA gene on cell volume in dinoflagellates vol.109, pp.None, 2020, https://doi.org/10.1016/j.hal.2021.102108
  7. Characterization of Two Zygnema Strains (Zygnema circumcarinatum SAG 698-1a and SAG 698-1b) and a Rapid Method to Estimate Nuclear Genome Size of Zygnematophycean Green Algae vol.12, pp.None, 2016, https://doi.org/10.3389/fpls.2021.610381
  8. Unlocking the Health Potential of Microalgae as Sustainable Sources of Bioactive Compounds vol.22, pp.9, 2016, https://doi.org/10.3390/ijms22094383