Effects of Cadmium on Growth, Photosynthetic Pigments, Photosynthetic Performance, Biochemical Parameters and Structure of Chloroplasts in the Agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales)

Rodrigo W. dos Santos, Éder C. Schmidt, Roberta de P. Martins, Alexandra Latini, Marcelo Maraschin, Paulo A. Horta, Zenilda L. Bouzon

Central Laboratory of Electron Microscopy, Federal University of Santa Catarina, Florianópolis, Brazil.
Department of Botany, Federal University of Santa Catarina, Florianópolis, Brazil.
Laboratório de Bioenergética e Estresse Oxidativo, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, Brazil.
Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina, Florianópolis, Brazil.
Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal Univer- sity of Santa Catarina, Florianópolis, Brazil.

DOI: 10.4236/ajps.2012.38129                

Abstract

This paper aimed to evaluate the effects of different concentrations of cadmium on growth rates, photosynthetic pigments, photosynthetic performance, biochemical parameters and structure of chloroplasts in G. domingensis. To accomplish this, apical segments of G. domingensis were cultivated with different concentrations of cadmium, ranging from 100 to 300 μM, over a period of 16 days, and were processed for transmission electron microscopy analysis. The plants exposed to cadmium showed chloroplast alteration, especially degeneration of thylakoids and a decrease in the concentration of photosynthetic pigments, such as chlorophyll a and phycobiliproteins. However, the volume of plastoglobuli increased. As a defense mechanism, the plants treated with cadmium showed an increase in glutathione reductase activity. These results agree with the decreased photosynthetic performance and relative electron transport rate observed after exposure of algae to cadmium. Taken together, these findings strongly indicate that cadmium negatively affects the ultrastructure and metabolism of the agarophyte G. domingensis, thus posing a threat to the economic vitality of this red macroalga.

Keywords

Gracilaria domingensis; Heavy Metals; Cadmium; Thylakoids; Photosynthetic Pigments; Antioxidant Systems

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	I. Rocchetta, P. I. Leonardi, G. M. Amado Filho, M. del C. R. de Molina and V. Conforti, “Ultrastructure and X-ray Microanalysis of Euglena Gracilis (Euglenophyta) under Chromium Stress,” Phycologia, Vol. 46, No. 3, 2007, pp. 300-306.
[2]	H. B. Pratap, F. A. Mamboya, M. S. P. Mtolera and M. Bj?rk, “The Effect of Copper on the Daily Growth Rate and Photosynthetic Efficiency of the Brown Macroalga Padina Boergensenii,” Proceedings of the Conference on Advances on Marine Sciences in Tanzania, Bilateral Marine Science Programme, 1999, pp. 185-192.
[3]	P. X. Sheng, Y. Ting, J. P. Chen and L. Hong, “Sorption of Lead, Copper, Cadmium, Zinc and Nickel by Marine Algal Biomass: Characterization of Biosorptive Capacity and Investigation of Mechanisms,” Journal of Colloid and Interface Science, Vol. 275, No. 1, 2004, pp. 131-141.
[4]	S. X. Hu, C. H. Tang and M. Wu, “Cadmium Accumulation by Several Seaweeds,” Science of the Total Environment, Vol. 187, No. 2, 1996, pp. 65-71. doi:10.1016/0048-9697(96)05143-1
[5]	M. Kumar, P. Kumari, V. Gupta, P. A. Anisha, C. R. K. Reddy and B. Jha, “Differential Responses to Cadmium Induced Oxidative Stress in Marine Macroalga Ulva Lactuca (Ulvales, Chlorophyta),” Biometals, Vol. 23, No. 2, 2010, pp. 315-325.
[6]	Z. L. Bouzon, E. C. Schmidt, A. C. de Almeida, N. S. Yokoya, M. C. de Oliveira and F. Y. Chow, “Cytochemical Characterization and Ultrastructural Organization in Calluses of the Agarophyte Gracilariopsis Tenuifrons (Gracilariales, Rhodophyta)”, Micron, Vol. 42, No. 1, 2011, pp. 80-86. doi:10.1016/j.micron.2010.07.012
[7]	L. Talarico, “Fine Structure and X-Ray Microanalysis of a Red Macrophyte Cultured under Cadmium Stress,” Environmental Pollution, Vol. 120, No. 3, 2002, pp. 813-821. doi:10.1016/S0269-7491(02)00156-2
[8]	B. E. Diannelidis and S. G. Delivopoulos, “The Effects of Zinc, Copper and Cadmium on the Fine Structure of Ceramium Ciliatum (Rhodophyceae, Ceramiales),” Marine Environmental Research, Vol. 44, No. 2, 1997, pp. 127-134. doi:10.1016/S0141-1136(96)00106-7
[9]	I. Visviki and J. W. Rachlin, “Ultrastructural Changes in Dunaliella Minuta Following Acute and Chronic Exposure to Copper and Cadmium,” Archives of Environmental Contamination and Toxicology, Vol. 23, No. 4, 1992, pp. 420-425.
[10]	L. R. Andrade, M. Farina, and G. M. Amado Filho, “Effects of Copper on Enteromorpha Flexuosa (Chlorophyta) in Vitro,” Ecotoxicology and Environmental Safety, Vol. 58, No. 1, 2004, pp. 117-125. doi:10.1016/S0147-6513(03)00106-4
[11]	L. R. de Andrade, M. Farina and G. M. A. Filho, “Role of Padina Gymnospora (Dictyotales, Phaeophyceae) Cell Walls in Cadmium Accumulation,” Phycologia, Vol. 41, No. 1, 2002, pp. 39-48.
[12]	M. A. Hashim and K. H. Chu, “Biosorption of Cadmium by Brown, Green and Red Seaweeds,” Chemical Engineering Journal, Vol. 97, No. 2-3, 2004, pp. 249-255. doi:10.1016/S1385-8947(03)00216-X
[13]	E. Pinto, T. C. S. Sigaud-Kutner, M. A. S. Leit?o, O. K. Okamoto, D. Morse and P. Colepicolo, “Heavy MetalInduced Oxidative Stress in Algae,” Journal of Phycology, Vol. 39, No. 6, 2003, pp. 1008-1018.
[14]	E. C. Oliveira and E. M. Plastino, “Gracilariaceae,” In: I. Akatsuka, Ed., Biology of Economic Algae, SPB Academic Publishing, The Hague, 1994, pp. 185-226.
[15]	R. Armisen and A. Postal, “World-Wide Use and Importance of Gracilaria,” Journal of Applied Phycology, Vol. 7, No. 3, 1995, pp. 231-243.
[16]	J. M. Kain and C. Destombe, “A Review of the Life History, Reproduction and Phenology of Gracilaria,” Journal of Applied Phycology, Vol. 7, No. 3, 1995, pp. 269-281.
[17]	E. C. Schmidt, R. Santos, P. A. Horta, M. Maraschin and Z. L. Bouzon, “Effects of UVB Radiation on the Agarophyte Gracilaria Domingensis (Rhodophyta, Gracilariales): Changes in Cell Organization, Growth and Photosynthetic Performance,” Micron, Vol. 41, No. 8, 2010, pp. 919-930. doi:10.1016/j.micron.2010.07.010
[18]	E. C. Oliveira, E. J. Paula, E. M. Plastino and R. Petti, “Metodologías Para el Cultivo no Axenico de Macroalgas Marinas in Vitro,” In: K. Alveal, M. Ferrario, E. Oliveira and E. SAR, Eds., Manual de Métodos Ficológicos, Universidad de Concepción, Concepción-Chile, 1995, pp. 429-447.
[19]	P. Edwards, “Illustrated Guide to the Seaweeds and Sea Grasses in the Vicinity of Porto Arkansas,” In: Dr. Tracy and A. Villareal, Eds., Contributions in Marine Science, Marine Science Institute, Texas, 1970, pp. 1-228.
[20]	L. Talarico, S. Bozo and G. Maranzana, “Preliminary Observations on Audouinella Saviana (Meneghini) Woelkerling (Nemaliales, Rhodophyta) Cultured at Increasing Cd Concentrations,” Phycologia, Vol. 36, 1997, p. 111.
[21]	J. R. Xia, Y. J. Li, J. Lu and B. Chen, “Effects of Copper and Cadmium on Growth, Photosyntesis, and Pigment Content in Gracilaria Lemaneiformis,” Bulletin of Environmental Contamination and Toxicology, Vol. 73, No. 6, 2004, pp. 979-986.
[22]	C. A. Penniman, A. C. Mathieson and C. E. Penniman, “Reproductive Phenology and Growth of Gracilaria tikvahiae McLachlan (Gigartinales, Rhodophyta) in the Great Bay Estuary, New Hampshire,” Botanica Marina, Vol. 29, No. 2, 1986, pp. 147-154.
[23]	A. J. White and C. Critchley, “Rapid Light Curves: A New Fluorescence Method to Assess the State of the Photosynthetic Apparatus,” Photosynthesis Research, Vol. 59, No. 1, 1999, pp. 63-72.
[24]	R. J. Jones, T. Kildea and O. Hoegh-Gudberg, “PAM Chlorophyll Fluorometry: A New in Situ Technique for Stress Assessment in Scleractinian Corals, Used to Examine the Effect of Cyanide from Cyanide Fishing,” Marine Pollution Bulletin, Vol. 38, No. 10, 1999, pp. 864-874. doi:10.1016/S0025-326X(98)90160-6
[25]	T. Platt, C. L. Gallegos and W. G. Harrison, “Photoinhibition of Photosynthesis in Natural Assemblages of Marine Phytoplankton,” Journal of Marine Research, Vol. 38, 1980, pp. 687-701.
[26]	N. S. Yokoya, O. Necchi, A. P. Martins, S. F. Gonzalez and E. M. Plastino, “Growth Responses and Photosynthetic Characteristics of Wild and Phycoerythrin-Deficient Strains of Hypnea Musciformis (Rhodophyta),” Journal of Applied Phycology, Vol. 19, No. 3, 2007, pp. 197-205. doi:10.1007/s10811-006-9124-9
[27]	E. C. Schmidt, M. Maraschin and Z. L. Bouzon, “Effects of UVB Radiation on the Carragenophyte Kappaphycus Alvarezii (Rhodophyta, Gigartinales): Changes in Ultrastructure, Growth, and Photosynthetic Pigments,” Hydrobiologia, Vol. 649, No. 1, 2010, pp. 171-182. doi:10.1007/s10750-010-0243-6
[28]	J. D. Hiscox and G. F. Israelstam, “A Method for the Extraction of Chlorophyll from Leaf Tissue without Maceration,” Canadian Journal of Botany, Vol. 57, No. 12, 1979, pp. 1332-1334.
[29]	E. C. Schmidt, B. G. Nunes, M. Maraschin and Z. L. Bouzon, “Effect of Ultraviolet-B Radiation on Growth, Photosynthetic Pigments, and Cell Biology of Kappaphycus Alvarezii (Rhodophyta, Gigartinales) Macroalgae Brown Strain,” Photosynthetica, Vol. 48, No. 2, 2010, pp. 161-172.
[30]	A. R. Wellburn, “The Spectral Determination of Chlorophyll A and Chlorophyll B, as well as Total Carotenoids, Using Various Solvents with Spectrophotometers of Different Resolution,” Journal Plant Physiology, Vol. 144, No. 3, 1994, pp. 307-313.
[31]	T. A. Kursar, J. van Der Meer and R. S. Alberte, “Light-Harvesting System of the Red Alga Gracilaria tikvahiae,” Plant Physiology, Vol. 73, 1983, pp. 353-360.
[32]	I. Carlberg and B. Mannervik, “Glutathione Reductase,” Methods in Enzymology, Vol. 113, 1985, pp. 484-490.
[33]	E. C. Schmidt, B. Pereira, C. L. M. Pontes, R. dos Santos, F. Scherner, P. A. Horta, R. de P. Martins, A. Latini, M. Maraschin and Z. L. Bouzon, “Alterations in Architecture and Metabolism Induced by Ultraviolet Radiation-B in the Carragenophyte Chondracanthus teedei (Rhodophyta, Gigartinales),” Protoplasma, Vol. 249, No. 2, 2012, pp. 353-367. doi:10.1007/s00709-011-0286-1
[34]	A. Cassina and R. Radi, “Differential Inhibitory Action of Nitric Oxide and Peroxynitrite on Mitochondrial Electron Transport,” Archives of Biochemistry and Biophysics, Vol. 328, No. 2, 1996, pp. 309-316.
[35]	A. Latini, M. Rodriguez, R. B. Rosa, K. Scussiato, G. Leipnitz, D. R. de Assis, G. da C. Ferreira, C. Funchal, M. C. Jacques-Silva, L. Buzzin, R. Giugliani, A. Cassina, R. Radi and M. Wajner, “3-Hydroxyglutaric Acid Moderately Impairs Energy Metabolism in Brain of Young Rats,” Neuroscience, Vol. 135, No. 1, 2005, pp. 111-120.
[36]	O. H. Lowry, N. J. Rosebough, A. L. Farr and R. J. Randall, “Protein Measurement with the Folin Phenol Reagent,” The Journal of Biological Chemistry, Vol. 193, No. 1, 1951, pp. 265-275.
[37]	E. C. Schmidt, L. A. Scariot, T. Rover and Z. L. Bouzon, “Changes in Ultrastructure and Histochemistry of Two Red Macroalgae Strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a Consequence of Ultraviolet B Radiation Exposure,” Micron, Vol. 40, No. 8, 2009, pp. 860-869.
[38]	E. S. Reynolds, “The Use of Lead Citrate at High pH as an Electron Opaque Stain in Electron Microscopy,” The Journal of Cell Biology, Vol. 17, No. 1, 1963, pp. 208-212.
[39]	J. Collén, E. Pinto, M. Pedersén and P. Colepicolo, “Induction of Oxidative Stress in the Red Macroalga Gracilaria tenuistipitata by Pollutant Metals,” Archives of Environmental Contamination and Toxicology, Vol. 45, No. 3, 2003, pp. 337-342.
[40]	M. Greger and E. Ogren, “Direct and Indirect Effects of Cd2+ on Photosynthesis in Sugar Beet (Beta vulgaris),” Plant Physiology, Vol. 83, No. 1, 1991, pp. 129-135.
[41]	A. K. Stobart, W. T. Griffiths, I. Ameen-Bukhari and R. P. Sherwood, “The Effects of Cd2+ on the Biosynthesis of Chlorophyll in Leaves of Barley,” Physiology Plantarum, Vol. 63, No. 3, 1985, pp. 293-298.
[42]	A. Holzinger, M. Y. Roleda and C. Lütz, “The Vegetative Arctic Freshwater Green Alga Zygnema Is Insensitive to Experimental UV Exposure,” Micron, Vol. 40, No. 8, 2009, pp. 831-838.