Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-17T13:19:15.418Z Has data issue: false hasContentIssue false
  • English
  • Français

The Effects of Lead and Copper on the Cellular Architecture and Metabolism of the Red Alga Gracilaria domingensis

Published online by Cambridge University Press:  03 April 2013

Claudiane Gouveia ,
Marianne Kreusch ,
Éder C. Schmidt ,
Marthiellen R. de L. Felix ,
Luz K.P. Osorio ,
Debora T. Pereira ,
Rodrigo dos Santos ,
Luciane C. Ouriques ,
Roberta de Paula Martins  and
Alexandra Latini
...Show all authors
Claudiane Gouveia
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Marianne Kreusch
Affiliation:
Scientific Initiation-PIBIC-CNPq, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Éder C. Schmidt*
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Marthiellen R. de L. Felix
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Luz K.P. Osorio
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Debora T. Pereira
Affiliation:
Scientific Initiation-PIBIC-CNPq, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Rodrigo dos Santos
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Luciane C. Ouriques
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Roberta de Paula Martins
Affiliation:
Laboratório de Bioenergética e Estresse Oxidativo, Department of Biochemistry, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Alexandra Latini
Affiliation:
Laboratório de Bioenergética e Estresse Oxidativo, Department of Biochemistry, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Fernanda Ramlov
Affiliation:
Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Tiago José G. Carvalho
Affiliation:
Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Fungyi Chow
Affiliation:
Institute of Bioscience, University of São Paulo, CEP 05508-090, São Paulo, SP, Brazil
Marcelo Maraschin
Affiliation:
Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Zenilda L. Bouzon
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil Central Laboratory of Electron Microscopy, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
*
*Corresponding author. E-mail: edcash@ccb.ufsc.br
Get access

Abstract

The effect of lead and copper on apical segments of Gracilaria domingensis was examined. Over a period of 7 days, the segments were cultivated with concentrations of 5 and 10 ppm under laboratory conditions. The samples were processed for light, confocal, and electron microscopy, as well as histochemistry, to evaluate growth rates, mitochondrial activity, protein levels, chlorophyll a, phycobiliproteins, and carotenoids. After 7 days of exposure to lead and copper, growth rates were slower than control, and biomass loss was observed on copper-treated plants. Ultrastructural damage was primarily observed in the internal organization of chloroplasts and cell wall thickness. X-ray microanalysis detected lead in the cell wall, while copper was detected in both the cytoplasm and cell wall. Moreover, lead and copper exposure led to photodamage of photosynthetic pigments and, consequently, changes in photosynthesis. However, protein content and glutathione reductase activity decreased only in the copper treatments. In both treatments, decreased mitochondrial NADH dehydrogenase activity was observed. Taken together, the present study demonstrates that (1) heavy metals such as lead and copper negatively affect various morphological, physiological, and biochemical processes in G. domingensis and (2) copper is more toxic than lead in G. domingensis.

Keywords

Gracilaria domingensisheavy metalmorphologyphotosynthetic pigmentsbiochemical response
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 3 , June 2013 , pp. 513 - 524
Copyright
Copyright © Microscopy Society of America 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1

†Claudiane Gouveia, Marianne Kreusch, and Éder C. Schmidt should be considered as first authors.

References

Andrade, L.R., Farina, M. & Amado Filho, G.M. (2002). Role of Padina gymnospora (Dictyotales, Phaeophyceae) cell walls in cadmium accumulation. Phycologia 41, 39–48.CrossRefGoogle Scholar
Andrade, L.R., Farina, M. & Amado Filho, G.M. (2004). Effects of copper on Enteromorpha flexuosa (Chlorophyta) in vitro. Ecotoxicol Environ Saf 58, 117–125.CrossRefGoogle ScholarPubMed
Bandy, B. & Davison, A.J. (1990). Mitochondrial mutations may increase oxidative stress: Implications for carcinogenesis and aging? Free Radic Biol Med 8, 523–539.CrossRefGoogle ScholarPubMed
Bouzon, Z.L., Ferreira, E.C., Santos, R., Scherner, F., Horta, P.A., Maraschin, M. & Schmidt, E.C. (2012). Influences of cadmium on fine structure and metabolism of Hypnea musciformis (Rhodophyta, Gigartinales) cultivated in vitro. Protoplasma 249, 637–650.CrossRefGoogle ScholarPubMed
Boveris, A., Cadenas, E. & Stoppani, A.O. (1976). Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem J 156, 435–444.CrossRefGoogle ScholarPubMed
Callow, M.E. & Callow, J. (2002). Marine biofouling: A sticking problem. Biologist 49, 1–5.Google Scholar
Carlberg, I. & Mannervik, B. (1985). Glutathione reductase. Methods Enzimol 113, 484–490.CrossRefGoogle ScholarPubMed
Cassiana, A. & Radi, R. (1996). Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transmit. Arch Biochem 328, 309–316.CrossRefGoogle Scholar
Chen, Q., Vazquez, E.J., Moghaddas, S., Hoppel, C.L. & Lesnefsky, E.J. (2003). Production of reactive oxygen species by mitochondria: Central role of complex III. J Biol Chem 278, 36027–36031.CrossRefGoogle ScholarPubMed
Collén, J., Pinto, E., Pedersén, M. & Colepicolo, P. (2003). Induction of oxidative stress in the red macroalgae Gracilaria tenuistipitata by polluant metals. Arch Environ Contam Toxicol 45, 337–342.CrossRefGoogle Scholar
Diannelidis, B. & Delivopoulos, S.G. (1997). The effects of zinc, copper and cadmium on the fine structure of Ceramium ciliatum (Rhodophyceae, Ceramiales). Mar Environ Res 44(2), 127–134.CrossRefGoogle Scholar
Edwards, P. (1970). Illustrated guide to the seaweeds and sea grasses in the vicinity of Porto Aransas. Texas Contrib Mar Sci 15, 1–228.Google Scholar
Eick, M.J., Peak, J.D., Brady, P.V. & Pesek, J.D. (1999). Kinetics of lead adsorption and desorption on goethite: Residence time effect. J Soil Sci 164, 28–39.CrossRefGoogle Scholar
Gantt, E. (1981). Phycobilisomes. Annu Rev Plant Physiol 32, 327–347.CrossRefGoogle Scholar
Guimarães, G.M., Plastino, E.M. & Oliveira, E.C. (1999). Life history reproduction and growth of Gracilaria domingensis (Gracilariales, Rhodophyta) from Brasil. Bot Mar 42, 481–486.CrossRefGoogle Scholar
Hausladen, A. & Fridovich, I. (1994). Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J Biol Chem 269, 29405–29408.CrossRefGoogle ScholarPubMed
Hepler, P.K. & Gunning, B.E.S. (1998). Confocal fluorescence microscopy of plant cells. Protoplasma 201, 121–157.CrossRefGoogle Scholar
Hiscox, J.D. & Israelstam, G.F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57, 1332–1334.CrossRefGoogle Scholar
Hu, S., Tang, C.H. & Wu, M. (1996). Cadmium accumulation by several seaweeds. Sci Total Environ 187, 65–71.CrossRefGoogle Scholar
Hulshof, P.J.M., Kosmeijer-Schuil, T., West, C.E. & Hollman, P.C.H. (2007). Quick screening of maize kernels for provitamin A content. J Food Comp Anal 20, 655–661.CrossRefGoogle Scholar
Kuhnen, S., Lemos, P.M.M., Campestrini, L.H., Ogliari, J.B., Dias, P.F. & Maraschin, M. (2009). Antiangiogenic properties of carotenoids: A potential role of maize as functional food. J Funct Foods 1, 284–290.CrossRefGoogle Scholar
Kursar, T.A., van Der Meer, J. & Alverte, R.S. (1983). Light-harvesting system of the red alga Gracilaria tikvahiae. II. Phycobilisome characteristics of pigment mutants. Plant Physiol 73, 361–369.CrossRefGoogle ScholarPubMed
Latini, A., Rodriguez, M., Borba Rosa, R., Scussiato, K., Leipnitz, G., Reir de Assis, D., da Costa Ferreira, G., Funchal, C., Jacques-Silva, MC., Buzin, L., Giugliani, R., Cassiana, A., Radi, R. & Wajner, M. (2005). 3-Hydroxyglutaric acid moderately impairs energy metabolism in brain of young rats. Neuroscience 135, 111–120.CrossRefGoogle ScholarPubMed
Lee, T.M., Chang, Y.C. & Lin, Y.H. (1999). Differences in physiological responses between winter and summer Gracilaria tenuistipitata (Gigartinales, Rhodophyta) to varying temperature. Bot Bull Acad Sin 40, 93–100.Google Scholar
Lowry, O.H., Rosebough, N.G. & Farr, A.L. (1951). Protein measurement with the folin phenol reagent. J Biol Chem 193, 265–275.CrossRefGoogle ScholarPubMed
Mallick, N. & Rai, L.C. (2001). Physiological responses of non-vascular plants to heavy metals. In Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants, Prasad, M.N.V. & Strzalka, K. (Eds.), pp. 111–147. Dordrecht, The Netherlands: Kluwer Publishers.Google Scholar
Mamboya, F.A., Pratap, H.B., Mtolera, M. & Bjork, M. (1999). The effect of copper on the daily growth rate and photosynthetic efficiency of the brown macroalgae Padina boergesenii . In Proceedings of the Conference on Advances on Marine Sciences in Tanzania, Richmond, M.D. & Francis, J. (Eds.), pp. 185–192.Google Scholar
Ologuin, M.M., Roa, E.C. & Uy, W.H. (2009). In vitro lead accumulation in Gracilaria coronopifolia and Gracilaria eucheumoides . J Environ Aquatic Res 1, 87–98.Google Scholar
Penniman, C.A., Mathieson, A.C. & Penniman, C.E. (1986). Reproductive phenology and growth of Gracilaria tikvahiae McLachlan (Gigartinales, Rhodophyta) in the Great Bay Estuary New Hampshire. Bot Mar 29, 147–154.CrossRefGoogle Scholar
Pinto, E., Carvalho, A.P., Cardozo, K.H.M., Malcata, F.X., dos Anjos, F.M. & Colepicolo, P. (2011). Effects of heavy metals and light levels on the biosynthesis of carotenoids and fatty acids in the macroalgae Gracilaria tenuistipitata (var. liui Zhang & Xia). Rev Bras Farmacogn 21, 349–354.CrossRefGoogle Scholar
Rocchetta, I., Leonardi, P.I., Amado Filho, G., Molina, M.C.R. & Conforti, V. (2007). Ultrastructure and X-ray microanalysis of Euglena gracilis (Euglenophyta) under chromium stress. Phycologia 46, 300–306.CrossRefGoogle Scholar
Santos, R., Schmidt, E.C., Paula, M.R., Latini, A., Horta, P.A., Maraschin, M. & Bouzon, Z.L. (2012). Effects of cadmium on growth, photosynthetic pigments, photosynthetic performance, biochemical parameters and structure of chloroplasts in the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales). Am J Plant Sci 3, 1077–1084.CrossRefGoogle Scholar
Schmidt, E.C., dos Santos, R. & Horta, P.A. (2010a). Effects of UVB radiation on the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales): Changes in cell organization, growth and photosynthetic performance. Micron 41, 919–930.CrossRefGoogle ScholarPubMed
Schmidt, E.C., Maraschin, M. & Bouzon, Z.L. (2010b). Effects of UVB radiation on the carragenophyte Kappaphycus alvarezii (Rhodophyta, Gigartinales): Changes in ultrastructure, growth, and photosynthetic pigments. Hydrobiologia 649, 171–182.CrossRefGoogle Scholar
Schmidt, E.C., Nunes, B.G., Maraschin, M. & Bouzon, Z.L. (2010c). Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain. Photosynthetica 48, 161–172.CrossRefGoogle Scholar
Schmidt, E.C., Pereira, B., Pontes, C.L.M., Santos, R., Scherner, F., Horta, P.A., Paula, M.R., Latini, A., Maraschin, M. & Bouzon, Z.L. (2012a). Alterations in architecture and metabolism induced by ultraviolet radiation-B in the carragenophyte Chondracanthus teedei (Rhodophyta, Gigartinales). Protoplasma 249, 353–367.CrossRefGoogle ScholarPubMed
Schmidt, E.C., Pereira, B., Santos, R., Gouveia, C., Costa, G.B., Faria, G.S.M., Scherner, F., Horta, P.A., Paula, M.R., Latini, A., Ramlov, F., Maraschin, M. & Bouzon, Z.L. (2012b). Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquatic Bot 100, 8–17.CrossRefGoogle Scholar
Schmidt, E.C., Santos, R., Faveri, C., Horta, P.A., Paula, M.R., Latini, A., Ramlov, F., Maraschin, M. & Bouzon, Z.L. (2012c). Response of the agarophyte Gelidium floridanum after in vitro exposure to ultraviolet radiation B: Changes in ultrastructure, pigments, and antioxidant systems. J Appl Phycol 24, 1341–1352.CrossRefGoogle Scholar
Schmidt, E.C., Scariot, L.A., Rover, T. & Bouzon, Z.L. (2009). Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure. Micron 40, 860–869.CrossRefGoogle ScholarPubMed
Scott, C.E. & Eldridge, A.L. (2005). Comparison of carotenoid content in fresh, frozen and canned corn. J Food Comp Anal 18, 551–559.CrossRefGoogle Scholar
Sharma, P. & Dubey, R.S. (2005). Lead toxicity in plants. Braz J Plant Physiol 17, 35–52.CrossRefGoogle Scholar
Sheng, P.X., Ting, Y., Chen, J.P. & Hong, L. (2004). Sorption of lead, copper, cadmium, zinc and nickel by marine algal biomass: Characterization of biosorptive capacity and investigation of mechanisms. J Colloid Interface Sci 275, 131–141.CrossRefGoogle ScholarPubMed
Talarico, L. (1996). Phycobiliproteins and phycobilisomes in red algae: Adaptative responses to light. Sci Mar 60, 205–222.Google Scholar
Talarico, L. (2002). Fine structure and X-ray microanalysis of a red macrophyte cultured under cadmium stress. Environ Pollut 120, 813–821.CrossRefGoogle ScholarPubMed
Tonon, A.P., Oliveira, M.C., Soriano, E.M. & Colepicolo, P. (2011). Absorption of metals and characterization of chemical elements present in three species of Gracilaria (Gracilariaceae) Greville: A genus of economical importance. Rev Bras Farmacogn 21, 355–360.CrossRefGoogle Scholar
Torres, M.A., Barros, M.P., Campos, S.C.G., Pinto, E., Rajamani, S., Sayre, R.T. & Colepicolo, P. (2008). Biochemical biomarkers in algae and marine pollution: A review. Ecotoxicol Environ Saf 71, 1–15.CrossRefGoogle ScholarPubMed
Tseng, C.K. (2001). Algal biotechnology industries and research activities in China. J Appl Phycol 13, 375–380.CrossRefGoogle Scholar
Turrens, J.F. (1997). Superoxide production by the mitochondrialrespiratory chain. Biosci Rep 17, 3–8.CrossRefGoogle Scholar
Turrens, J.F. & Boveris, A. (1980). Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191, 421–427.CrossRefGoogle ScholarPubMed
Visviki, I. & Rachlin, J.W. (1992). Ultrastructural changes in Dunaliella minuta following acute and chronic exposure to copper and cadmium. Arch Environ Contam Toxicol 23, 420–425.CrossRefGoogle ScholarPubMed
Wellburn, A.R. (1994). The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144, 307–313.CrossRefGoogle Scholar
Xia, J.R., Li, Y.J., Lu, J. & Chen, B. (2004). Effects of copper and cadmium on growth, photosynthesis, and pigment content in Gracilaria lemaneiformis. Bull Environ Contam Toxicol 73, 979–986.CrossRefGoogle ScholarPubMed
Yruela, I. (2005). Copper in plants. Braz J Plant Physiol 17, 145–146.CrossRefGoogle Scholar
Zhang, Y., Marcillat, O., Giulivi, C., Ernster, L. & Davies, K.J. (1990). The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J Biol Chem 265, 16330–16336.CrossRefGoogle ScholarPubMed