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Assessment of Heavy Metal Effects on the Freshwater Microalga, Chlorella vulgaris, by Chlorophyll Fluorescence Analysis

엽록소형광분석을 이용한 담수산 클로렐라(Chlorella vulgaris)에 미치는 중금속의 영향 평가

  • Oh, Soon-Ja (Research Institute of Climate Change and Agriculture, RDA) ;
  • Koh, Seok-Chan (Department of Biology and Research Institute for Natural Sciences, Jeju National University)
  • 오순자 (농촌진흥청 온난화대응농업연구소) ;
  • 고석찬 (제주대학교 생물학과.기초과학연구소)
  • Received : 2015.07.26
  • Accepted : 2015.11.26
  • Published : 2015.12.29

Abstract

The response of the freshwater microalga, Chlorella vulgaris, to heavy metal stress was examined based on chlorophyll fluorescence analysis to assess the toxic effects of heavy metals in freshwater ecosystems. When toxic effects were analyzed using regular chlorophyll fluorescence analysis, photosystem II activity($F_v/F_m$) decreased significantly when exposed to $Cu^{2+}$ and $Hg^{2+}$ for 12 h, and decreased in the order of $Hg^{2+}>Cu^{2+}>Cd^{2+}>Ni^{2+}$ when exposed for 24h. The effective photochemical quantum yield(${\phi}{\prime}_{PSII}$), chlorophyll fluorescence decrease ratio($R_{Fd}$), minimal fluorescence yield($F_o$), and non-photochemical quenching(NPQ), but not photochemical quenching(qP), responded sensitively to $Hg^{2+}$, $Cu^{2+}$, and $Cd^{2+}$. These results suggest that $F_v/F_m$, as well as ${\phi}{\prime}_{PSII}$, $R_{Fd}$, $F_o$, and NPQ could be used to assess the effects of heavy metal ions in freshwater ecosystems. However, because many types of heavy metal ions and toxic compounds co-occur under natural conditions, it is difficult to assess heavy metal toxicity in freshwater ecosystems. When Chlorella was exposed to heavy metal ions for 12 or 24h, $F_v/F_m$ and maximal fluorescence yield($F_m$) changed in response to $Hg^{2+}$ and $Cu^{2+}$ based on image analysis. However, assessing quantitatively the toxic effects of several heavy metal ions is challenging.

Keywords

Chlorella vulgaris;Heavy metal ions;Image analysis;Photosystem II activity($F_v/F_m$)

Acknowledgement

Supported by : 제주대학교

References

  1. Shrotri, C., Rathore, V., Mohanty, P., 1981, Studies on photosynthetic electron transport, photophosphorylation and $CO_2$ fixation in $Zn^{2+}$ deficient leaf cells of Zea mays, J. Plant Nutri., 3, 945-954. https://doi.org/10.1080/01904168109362890
  2. Strasser, B. J., Strasser, R. J., 1995, Measuring fast fluorescence transients to address environmental questions: The JIP test, in: Mathis, P. (ed.), Photosynthesis: From Light to Biosphere, Kluwer Academic, Dordrecht, 977-980.
  3. Thompson, A. S., Rhodes, J. C., Pettman, I., 1988, Culture collection of algae and protozoa catalogue of strains, Published by CCAP, Cumbria, UK, 164.
  4. Travieso, L., Canizares, R. O., Borja, R., Benitez, F., Dominguez, A. R., Dupeyron, R., Valiente, V., 1999, Heavy metal removal by microalgae, Bull. Environ. Contam. Toxicol., 62, 144-151. https://doi.org/10.1007/s001289900853
  5. Ulloa, G., Otero, A., Sanchez, M., Sineiro, J., Nunez, M. J., Fabregas, J., 2012, Effect of Mg, Si, and Sr on growth and antioxidant activity of the marine microalga Tetraselmis suecica, J. Appl. Phycol., 24, 1229-1236. https://doi.org/10.1007/s10811-011-9764-2
  6. US Environmental Protection Agency, 1996, Algal toxicity tiers I and II. Series 850 Ecological effects test guidelines, Washington DC.
  7. Wan, G., Najeeb, U., Jilani, G., Naeem, M. S., Zhou, W., 2011, Calcium invigorates the cadmium-stressed Brassica napus L. plant by strengthening their photosynthetic system, Environ. Sci. Pollut. Res., 18, 1478-1486. https://doi.org/10.1007/s11356-011-0509-1
  8. Lichtenthaler, H. K., Langsdorf, G., Lenk, S., Buschmann, C., 2005, Chlorophyll fluorescence imaging of photosynthetic activity with the flash-lamp fluore-scence imaging system, Photosynthetica, 43, 355-369. https://doi.org/10.1007/s11099-005-0060-8
  9. Lu, C. M., Chau, C. W., Zhang, J. H., 2000, Acute toxicity of excess mercury on the photosynthetic performance of cyanobacterium, S. platensis - assessment by chlorophyll fluorescence analysis, Chemosphere, 41, 191-196. https://doi.org/10.1016/S0045-6535(99)00411-7
  10. Maksymiec, W., Wojcik, M., Krupa, Z., 2007, Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate, Chemosphere, 66, 421-427. https://doi.org/10.1016/j.chemosphere.2006.06.025
  11. Mallick, N., Mohn, F. H., 2003, Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus, Ecotoxicol. Environ. Saf., 55, 64-69. https://doi.org/10.1016/S0147-6513(02)00122-7
  12. Nedbal, L., Soukupova, J., Whitmarsh, J., Trtilek, M., 2000, Posthavest imaging of chlorophyll fluorescence from lemons can be used to predict fruit quality, Photosynthetica, 38, 571-579. https://doi.org/10.1023/A:1012413524395
  13. Oh, S., Koh, S. C., 2013, Chlorophyll a fluorescence response to mercury stress in the freshwater microalga Chlorella vulgaris, J. Environ. Sci., 22, 705-715 (in Korean).
  14. Organisation for Economic Cooperation and Development, 1984, Algal growth inhibition test. OECD guidelines for testing of chemicals 201, Paris, France.
  15. Plekhanov, S. E., Chemeris, Y. K., 2003, Early toxic effects of zinc, cobalt and cadmium on photosynthetic activity of the green alga Chlorella pyrenoidosa Chick S-39, Biol. Bul., 30, 506-511. https://doi.org/10.1023/A:1025806921291
  16. Ricart, M., Guasch, H., Barcelo, D., Brix, R., Conceicao, M. H., Geiszinger, A., Lopez de Alda, M. J., Lopez-Doval, J. C., Munoz, I., Postigo, C., Romani, A. M., Villagrasa, M., Sabater, S., 2010, Primary and complex stressors in polluted Mediterranean rivers: pesticide effects on biological communities, J. Hydrol., 383, 52-61. https://doi.org/10.1016/j.jhydrol.2009.08.014
  17. Rysgaard, S., Kuhl, M., Glud, R. N., Hansen, J. W., 2001, Biomass, production and horizontal patchiness of sea ice algae in a high-Arctic fjord (Young Sound, NE Greenland), Mar. Ecol. Prog. Ser., 223, 15-26. https://doi.org/10.3354/meps223015
  18. Schreiber, U., Schliwa, U., Bilger, W., 1986, Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer, Photosynth. Res., 10, 51-62. https://doi.org/10.1007/BF00024185
  19. Serodio, J., Silva, J. M., Catarino, F., 1997, Nondestructive tracing of migratory rhythms of intertidal benthic microalgae using in vivo chlorophyll a fluorescence, J. Phycol., 33, 542-553. https://doi.org/10.1111/j.0022-3646.1997.00542.x
  20. Jarvis, S. C., Jones, L. H. P., Hopper, M. J., 1976, Cadmium uptake from solution by plants and its transport from roots to shoots, Plant Soil., 44, 179-191. https://doi.org/10.1007/BF00016965
  21. Kupper, H., Kupper, F., Spiller, M., 1996, Environmental relevance of heavy metal substituted chlorophylls using the example of water plants, J. Exp. Bot., 47, 259-266. https://doi.org/10.1093/jxb/47.2.259
  22. Aruoja, V., Dubourguier, H. C., Kasemets, K., Kahru, A., 2009, Toxicity of nanoparticles of CuO, ZnO and $TiO_2$ to microalgae Pseudokirchneriella subcapitata, Sci. Total Environ., 407, 1461-1468. https://doi.org/10.1016/j.scitotenv.2008.10.053
  23. Balaknina, T., Kosobryukhov, A., Ivanov, A., Kres-lauskii, V., 2005, The effect of cadmium on $CO_2$ exchange, variable fluorescence of chlorophyll and the level of antioxidant enzymes in pea leaves, Russian J. Plant Physiol., 52, 15-20. https://doi.org/10.1007/s11183-005-0003-z
  24. Bilger, W., Bjorkman, O., 1990, Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis, Photosynth. Res., 25, 173-185. https://doi.org/10.1007/BF00033159
  25. Blinova, I., 2004, Use of freshwater algae and duckweeds for phytotoxicity testing, Environ. toxicol., 19, 425-428. https://doi.org/10.1002/tox.20042
  26. Bolhar-Nordenkampf, H. R., oquist, G., 1993, Chlorophyll fluorescence as a tool in photosynthesis research. In Photosynthesis and Production in a Changing Environment, in: Hall, D. O., Scurlock, J. M. O., Bolhar-Nordenkampf, H. R., Leegood, R. C., Long, S. P., (eds.), A Field and Laboratory Manual, Chapman and Hall, London, 193-206.
  27. Chaoui, A., Mazhoudi, S., Ghorbal, M. H., Elferjani, E., 1997, Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.), Plant Sci., 127, 139-147. https://doi.org/10.1016/S0168-9452(97)00115-5
  28. Clijsters, H., Van Assche, F., 1985, Inhibition of photosynthesis by heavy metals, Photosynth. Res., 7, 31-40. https://doi.org/10.1007/BF00032920
  29. Genty, B., Briantais, J. M., Baker, N. R., 1989, The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence, Acta Biochim. Biophys., 99, 87-92.
  30. Gilmore, A. M., 1997, Mechanistic aspects of xanthophyll cycle dependent photoprotection in higher plant chloroplasts and leaves, Physiol. Plant., 99, 197-209. https://doi.org/10.1111/j.1399-3054.1997.tb03449.x
  31. Horton, P., Ruban, A. V., Young, A. J., 1999, Regulation of the structure and function of the light harvesting complexes of photosytem II by the xanthophyll cycle. In the photochemistry of carotenoids, in: Frank, H. A., Young, A. J., Cogdell, R. J., (eds.), Kluwer, Dordrecht, 271-291.
  32. Huang, L., Xu, J., Li, T., Wang, L., Deng, T., Yu, X., 2014, Effects of additional $Mg^{2+}$ on the growth, lipid production, and fatty acid composition of Monoraphidium sp. FXY-10 under different culture conditions, Ann. Microbiol., 64, 1247-1256. https://doi.org/10.1007/s13213-013-0768-9
  33. Hwang, U. K., Ryu, H. M., Lee, J. W., Lee, S. M., Kang, H. S., 2014, Toxic effects of heavy metal (Cd, Cu, Zn) on population growth rate of the marine diatom (Skeletonema costatum), Korean J. Environ. Biol., 32, 243-249 (in Korean). https://doi.org/10.11626/KJEB.2014.32.3.243
  34. Aidid, S. B., Okamoto, H., 1992, Effects of lead, cadmium and zinc on the electric membrane potential at the xylem/symplast interface and cell elongation of Impatiens balsamina, Environ. Exp. Bot., 32, 439-448. https://doi.org/10.1016/0098-8472(92)90056-8
  35. An, Y. J., Nam, S. H., Lee, J. K., 2007, Domestic test species for aquatic toxicity assessment in Korea, Korean J. Limnol., 40, 1-13 (in Korean).