Table of Contents Author Guidelines Submit a Manuscript
The Scientific World Journal
Volume 2012 (2012), Article ID 982957, 15 pages
http://dx.doi.org/10.1100/2012/982957
Research Article

Zinc Affects Differently Growth, Photosynthesis, Antioxidant Enzyme Activities and Phytochelatin Synthase Expression of Four Marine Diatoms

1Mer, Molécules, Santé, EA 2160, LUNAM Université, Faculté des Sciences et Techniques, Université du Maine, Avenue Olivier Messiaen, 72085 Le Mans cedex 9, France
2Laboratory of Plant Physiology, Department of Biology, University of Education of Ho Chi Minh City, 5th District, 280 An Duong Vuong, Ho Chi Minh City, Vietnam
3Plant Physiology Department, Faculty of Biology, University of Natural Sciences, 227 Nguyen Van Cu, 5th District, Ho Chi Minh City, Vietnam

Received 28 October 2011; Accepted 10 January 2012

Academic Editor: Mahir D. Mamedov

Copyright © 2012 Thi Le Nhung Nguyen-Deroche et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Granum, J. A. Raven, and R. C. Leegood, “How do marine diatoms fix 10 billion tonnes of inorganic carbon per year?” Canadian Journal of Botany, vol. 83, no. 7, pp. 898–908, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. C. A. Atkins, B. D. Patterson, and D. Graham, “Plant carbonic anhydrases. II preparation and some properties of monocotyledon and dicotyledon enzyme types,” Plant Physiology, vol. 50, no. 2, pp. 218–223, 1972. View at Google Scholar
  3. J. L. Riechmann and O. J. Ratcliffe, “A genomic perspective on plant transcription factors,” Current Opinion in Plant Biology, vol. 3, no. 5, pp. 423–434, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. I. Flor-Parra, M. Vranes, J. Kämper, and J. Pérez-Martín, “Biz1, a zinc finger protein required for plant invasion by Ustilago maydis, regulates the levels of a mitotic cyclin,” Plant Cell, vol. 18, no. 9, pp. 2369–2387, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Bertrand and I. Poirier, “Photosynthetic organisms and excess of metals,” Photosynthetica, vol. 43, no. 3, pp. 345–353, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. J. L. Stauber and T. M. Florence, “Mechanism of toxicity of zinc to the marine diatom Nitzschia closterium,” Marine Biology, vol. 105, no. 3, pp. 519–524, 1990. View at Google Scholar · View at Scopus
  7. A. Cid, C. Herrero, E. Torres, and J. Abalde, “Copper toxicity on the marine microalga Phaeodactylum tricornutum: effects on photosynthesis and related parameters,” Aquatic Toxicology, vol. 31, no. 2, pp. 165–174, 1995. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Gagneux-Moreaux, Les métaux (Cd, Cu, Pb et Zn) dans la production des microalgues sur différents milieux de culture: biodisponibilité, bioaccumulation et impact physiologique, Ph.D. thesis, Nantes university, 2006.
  9. W. M. El-Sarraf and O. E. Taha, “Effets of copper on photosynthetic activity and chlorophyll-a content of Chaetoceros radicans Schütt,” Bulletin of the High Institute of Public Health, vol. 25, no. 2, pp. 439–446, 1995. View at Google Scholar
  10. T. L. N. Nguyen-Deroche, T. T. Le, T. V. Bui, Y. Rincé, G. Tremblin, and A. Morant-Manceau, “Effects of copper on growth and photosynthesis in marine diatoms: a comparison between species from two different geographical areas,” Cryptogamie, Algologie, vol. 30, no. 2, pp. 97–109, 2009. View at Google Scholar · View at Scopus
  11. M. Li, C. Hu, Q. Zhu, L. Chen, Z. Kong, and Z. Liu, “Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae),” Chemosphere, vol. 62, no. 4, pp. 565–572, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. J. W. Rijstenbil, J. W. M. Derksen, L. J. A. Gerringa et al., “Oxidative stress induced by copper: defense and damage in the marine planktonic diatom Ditylum brightwellii, grown in continuous cultures with high and low zinc levels,” Marine Biology, vol. 119, no. 4, pp. 583–590, 1994. View at Google Scholar · View at Scopus
  13. J. W. Rijstenbil, “Effects of UVB radiation and salt stress on growth, pigments and antioxidative defence of the marine diatom Cylindrotheca closterium,” Marine Ecology Progress Series, vol. 254, pp. 37–48, 2003. View at Google Scholar · View at Scopus
  14. D. Branco, A. Lima, S. F. P. Almeida, and E. Figueira, “Sensitivity of biochemical markers to evaluate cadmium stress in the freshwater diatom Nitzschia palea (Kützing) W. Smith,” Aquatic Toxicology, vol. 99, no. 2, pp. 109–117, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Solymosi and M. Bertrand , “Soil metals, chloroplasts, and secure crop production: a review,” Agronomy for Sustainable Environment, vol. 32, no. 1, pp. 245–272, 2010. View at Publisher · View at Google Scholar
  16. B. E. Imber, M. G. Robinson, A. M. Ortega, and J. D. Burton, “Complexation of zinc by exudates from Skeletonema costatum grown in culture,” Marine Chemistry, vol. 16, no. 2, pp. 131–139, 1985. View at Google Scholar · View at Scopus
  17. E. Grill, S. Loffler, E. L. Winnacker, and M. H. Zenk, “Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase),” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 18, pp. 6838–6842, 1989. View at Google Scholar
  18. F. Sylvestre, B. Beck-Eichler, W. Duleba, and J. P. Debenay, “Modern benthic diatom distribution in a hypersaline coastal lagoon: the lagoa de araruama (R.J.), Brazil,” Hydrobiologia, vol. 443, pp. 213–231, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Rech, J.-L. Mouget, A. Morant-Manceau, P. Rosa, and G. Tremblin, “Long-term acclimation to UV radiation: effects on growth, photosynthesis and carbonic anhydrase activity in marine diatoms,” Botanica Marina, vol. 48, no. 5-6, pp. 407–420, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Fouqueray, J. L. Mouget, A. Morant-Manceau, and G. Tremblin, “Dynamics of short-term acclimation to UV radiation in marine diatoms,” Journal of Photochemistry and Photobiology B, vol. 89, no. 1, pp. 1–8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. P. J. Harrison, R. E. Waters, and F. J. R. Taylor, “A broad spectrum artificial seawater medium for coastal and open ocean phytoplankton,” Journal of Phycology, vol. 16, no. 1, pp. 28–35, 1980. View at Publisher · View at Google Scholar
  22. B. J. Speziale, S. P. Schreiner, P. A. Giammatteo, and J. E. Schindler, “Comparison of N,N- dimethylformamide, dimethyl sulfoxide, and acetone for extraction of phytoplankton chlorophyll,” Canadian Journal of Fisheries and Aquatic Sciences, vol. 41, no. 10, pp. 1519–1522, 1984. View at Google Scholar · View at Scopus
  23. P. H. C. Eilers and J. C. H. Peeters, “A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton,” Ecological Modelling, vol. 42, no. 3-4, pp. 199–215, 1988. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Rech, J.-L. Mouget, and G. Tremblin, “Modification of the Hansatech FMS fluorometer to facilitate measurements with microalgal cultures,” Aquatic Botany, vol. 77, no. 1, pp. 71–80, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. J.-L. Mouget, G. Tremblin, A. Morant-Manceau, M. Morançais, and J. M. Robert, “Long-term photoacclimation of Haslea ostrearia (Bacillariophyta): effect of irradiance on growth rates, pigment content and photosynthesis,” European Journal of Phycology, vol. 34, no. 2, pp. 109–115, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Dionisio-Sese and S. Miyachi, “The effect of sodium chloride on carbonic anhydrase activity in marine microalgae,” Journal of Phycology, vol. 28, no. 5, pp. 619–624, 1992. View at Publisher · View at Google Scholar
  27. A. Morant-Manceau, T. L. N. Nguyen, E. Pradier, and G. Tremblin, “Carbonic anhydrase activity and photosynthesis in marine diatoms,” European Journal of Phycology, vol. 42, no. 3, pp. 263–270, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Aebi, “Catalase in vitro,” Methods in Enzymology, vol. 105, pp. 121–126, 1984. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Nakano and K. Asada, “Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts,” Plant and Cell Physiology, vol. 22, no. 5, pp. 867–880, 1981. View at Google Scholar · View at Scopus
  30. E. Morelli and G. Scarano, “Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutum,” Plant Science, vol. 167, no. 2, pp. 289–296, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. B. N. Tripathi, S. K. Mehta, A. Amar, and J. P. Gaur, “Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+,” Chemosphere, vol. 62, no. 4, pp. 538–544, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. E. F. Hartree, “Determination of protein: a modification of the lowry method that gives a linear photometric response,” Analytical Biochemistry, vol. 48, no. 2, pp. 422–427, 1972. View at Google Scholar · View at Scopus
  33. J. J. Doyle and J. L. Doyle, “Isolation of plant DNA from fresh tissue,” Focus, vol. 12, pp. 13–15, 1990. View at Google Scholar
  34. S. F. Altschul, W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, “Basic local alignment search tool,” Journal of Molecular Biology, vol. 215, no. 3, pp. 403–410, 1990. View at Publisher · View at Google Scholar · View at Scopus
  35. K. B. Nicholas and H. B. Nicholas, “GENEDOC a Tool for Editing and Annoting Multiple Sequence,” Alignments, 1997, http://www.psc.edu/biomed/genedoc.
  36. J. Sambrook, E. F. Fritsch, and T. Maniatis, Molecular Cloning: A laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA, 1989.
  37. H. Hu, Y. Shi, W. Cong, and Z. Cai, “Growth and photosynthesis limitation of marine red tide alga Skeletonema costatum by low concentrations of Zn2+,” Biotechnology Letters, vol. 25, no. 22, pp. 1881–1885, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Morelli and G. Scarano, “Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutum,” Marine Environmental Research, vol. 52, no. 4, pp. 383–395, 2001. View at Google Scholar · View at Scopus
  39. M. Lamote, E. Darko, B. Schoefs, and Y. Lemoine, “Assembly of the photosynthetic apparatus in embryos from Fucus serratus L.,” Photosynthesis Research, vol. 77, no. 1, pp. 45–52, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Kralova, E. Masarovicova, and K. Gyoryova, “The physiological response of green algae (Chlorella vulgaris) to pH-dependent inhibitory activity of some zinc(II) compounds: carboxylato- and halogenocarboxylatozinc(II) complexes,” Chemical Papers, vol. 58, no. 5, pp. 353–356, 2004. View at Google Scholar
  41. S. A. Shehata, M. R. Lasheen, G. H. Ali, and I. A. Kobbia, “Toxic effect of certain metals mixture on some physiological and morphological characteristics of freshwater algae,” Water, Air, and Soil Pollution, vol. 110, no. 1-2, pp. 119–135, 1999. View at Publisher · View at Google Scholar · View at Scopus
  42. N. S. Fisher, G. J. Jones, and D. M. Nelson, “Effects of copper and zinc on growth, morphology, and metabolism of Asterionella japonica (Cleve),” Journal of Experimental Marine Biology and Ecology, vol. 51, no. 1, pp. 37–56, 1981. View at Publisher · View at Google Scholar · View at Scopus
  43. H. H. Omar, “Bioremoval of zinc ions by Scenedesmus obliquus and Scenedesmus quadricauda and its effect on growth and metabolism,” International Biodeterioration and Biodegradation, vol. 50, no. 2, pp. 95–100, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Rai, A. Sing, and N. Mallick, “Studies on photosynthesis, the associated electron transport system and some physiological variables of Chlorella vulgaris under heavy metal stress,” Journal of Plant Physiology, vol. 137, no. 4, pp. 419–424, 1991. View at Publisher · View at Google Scholar
  45. S. I. Beale, “Enzymes of chlorophyll biosynthesis,” Photosynthesis Research, vol. 60, no. 1, pp. 43–73, 1999. View at Publisher · View at Google Scholar · View at Scopus
  46. R. A. Danilov and N. G. A. Ekelund, “Effects of Cu2+, Ni2+, Pb2+, Zn2+ and pentachlorophenol on photosynthesis and motility in Chlamydomonas reinhardtii in short-term exposure experiments,” The BMC Ecology, vol. 1, article 1, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Koukal, C. Guéguen, M. Pardos, and J. Dominik, “Influence of humic substances on the toxic effects of cadmium and zinc to the green alga Pseudokirchneriella subcapitata,” Chemosphere, vol. 53, no. 8, pp. 953–961, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Lefebvre, J.-L. Mouget, P. Loret, P. Rosa, and G. Tremblin, “Comparison between fluorimetry and oximetry techniques to measure photosynthesis in the diatom Skeletonema costatum cultivated under simulated seasonal conditions,” Journal of Photochemistry and Photobiology B, vol. 86, no. 2, pp. 131–139, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Kühl, R. N. Glud, J. Borum, R. Roberts, and S. Rysgaard, “Photosynthetic performance of surface-associated algae below sea ice as measured with a pulse-amplitude-modulated (PAM) fluorometer and O2 microsensors,” Marine Ecology Progress Series, vol. 223, pp. 1–14, 2001. View at Google Scholar · View at Scopus
  50. I. A. Flameling and J. Krompkamp, “Light dependence of quantum yields for PSII charge separation and oxygen evolution in eukaryotic algae,” Limnology and oceanography, vol. 43, no. 2, pp. 284–287, 1998. View at Google Scholar
  51. A. G. Roberts, M. K. Bowman, and D. M. Kramer, “Certain metal ions are inhibitors of cytochrome b6f complex “Rieske” iron-sulfur protein domain movements,” Biochemistry, vol. 41, no. 12, pp. 4070–4079, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Giachini, F. Francia, G. Veronesi et al., “X-ray absorption studies of Zn2+ binding sites in bacterial, avian, and bovine cytochrome bc1 complexes,” Biophysical Journal, vol. 93, no. 8, pp. 2934–2951, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Kügler, V. Kruft, U. K. Schmitz, and H.-P. Braun, “Characterization of the PetM subunit of the b6f complex from higher plants,” Journal of Plant Physiology, vol. 153, no. 5-6, pp. 581–586, 1998. View at Google Scholar · View at Scopus
  54. J. F. Allen, “Cytochrome b6f: structure for signalling and vectorial metabolism,” Trends in Plant Science, vol. 9, no. 3, pp. 130–137, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Bertrand, “Carotenoid biosynthesis in diatoms,” Photosynthesis Research, vol. 106, no. 1-2, pp. 89–102, 2010. View at Google Scholar · View at Scopus
  56. Y. Lemoine and B. Schoefs, “Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress,” Photosynthesis Research, vol. 106, no. 1-2, pp. 155–177, 2010. View at Google Scholar · View at Scopus
  57. M. Bertrand, B. Schoefs, P. Siffel, K. Rohacek, and I. Molnar, “Cadmium inhibits epoxidation of diatoxanthin to diadinoxanthin in the xanthophyll cycle of the marine diatom Phaeodactylum tricornutum,” The FEBS Letters, vol. 508, no. 1, pp. 153–156, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Rashid, E. L. Camm, and A. K. M. Ekramoddoullah, “Molecular mechanism of action of Pb2+ and Zn2+ on water oxidizing complex of photosystem II,” The FEBS Letters, vol. 350, no. 2-3, pp. 296–298, 1994. View at Publisher · View at Google Scholar · View at Scopus
  59. N. Vaillant, F. Monnet, A. Hitmi, H. Sallanon, and A. Coudret, “Comparative study of responses in four Datura species to a zinc stress,” Chemosphere, vol. 59, no. 7, pp. 1005–1013, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Subrahmanyam and V. S. Rathore, “Influence of manganese toxicity on photosynthesis in ricebean (Vigna umbellata) seedlings,” Photosynthetica, vol. 38, no. 3, pp. 449–453, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. W. G. Sunda and S. A. Huntsman, “Effect of CO2 supply and demand on zinc uptake and growth limitation in a coastal diatom,” Limnology and Oceanography, vol. 50, no. 4, pp. 1181–1192, 2005. View at Google Scholar · View at Scopus
  62. F. Monnet, N. Vaillant, P. Vernay, A. Coudret, H. Sallanon, and A. Hitmi, “Relationship between PSII activity, CO2 fixation, and Zn, Mn and Mg contents of Lolium perenne under zinc stress,” Journal of Plant Physiology, vol. 158, no. 9, pp. 1137–1144, 2001. View at Google Scholar · View at Scopus
  63. K. Aizawa and S. Miyachi, “Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria,” FEMS Microbiology Letters, vol. 39, no. 3, pp. 215–233, 1986. View at Google Scholar · View at Scopus
  64. D. Sültemeyer, C. Schmidt, and H. P. Fock, “Carbonic anhydrases in higher plants and aquatic microorganisms,” Physiologia Plantarum, vol. 88, no. 1, pp. 179–190, 1993. View at Publisher · View at Google Scholar
  65. J. V. Moroney, S. G. Bartlett, and G. Samuelsson, “Carbonic anhydrases in plants and algae,” Plant, Cell and Environment, vol. 24, no. 2, pp. 141–153, 2001. View at Publisher · View at Google Scholar · View at Scopus
  66. T. W. Lane and F. M. M. Morel, “Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii,” Plant Physiology, vol. 123, no. 1, pp. 345–352, 2000. View at Google Scholar · View at Scopus
  67. E. Pinto, T. C. S. Sigaud-Kutner, M. A. S. Leitao, O. K. Okamoto, D. Morse, and P. Colepicolo, “Heavy metal-induced oxidative stress in algae,” Journal of Phycology, vol. 39, no. 6, pp. 1008–1018, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. M. S. French and L. V. Evans, “The effects of copper and zinc on growth of the fouling diatoms Amphora and Amphiprora,” Biofouling, vol. 1, pp. 3–18, 1988. View at Google Scholar
  69. C. Cobbett and P. Goldsbrough, “Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis,” Annual Review of Plant Biology, vol. 53, pp. 159–182, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. N. Tsuji, N. Hirayanagi, O. Iwabe et al., “Regulation of phytochelatin synthesis by zinc and cadmium in marine green alga, Dunaliella tertiolecta,” Phytochemistry, vol. 62, no. 3, pp. 453–459, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. J. F. Souza and W. E. Rauser, “Maize and radish sequester excess cadmium and zinc in different ways,” Plant Science, vol. 165, no. 5, pp. 1009–1022, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. S. K. Kawakami, M. Gledhill, and E. P. Achterberg, “Production of phytochelatins and glutathione by marine phytoplankton in response to metal stress,” Journal of Phycology, vol. 42, no. 5, pp. 975–989, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. K. Hirata, Y. Tsujimoto, T. Namba et al., “Strong induction of phytochelatin synthesis by zinc in marine green alga, Dunaliella tertiolecta,” Journal of Bioscience and Bioengineering, vol. 92, no. 1, pp. 24–29, 2001. View at Publisher · View at Google Scholar · View at Scopus