Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-18T19:03:41.918Z Has data issue: false hasContentIssue false
  • English
  • Français

The Effect of Cadmium Under Different Salinity Conditions on the Cellular Architecture and Metabolism in the Red Alga Pterocladiella capillacea (Rhodophyta, Gelidiales)

Published online by Cambridge University Press:  01 July 2014

Marthiellen R. de L. Felix ,
Luz K.P. Osorio ,
Luciane C. Ouriques ,
Francine L. Farias-Soares ,
Neusa Steiner ,
Marianne Kreusch ,
Debora T. Pereira ,
Carmen Simioni ,
Giulia B. Costa  and
Paulo A. Horta
...Show all authors
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
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
Francine L. Farias-Soares
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Neusa Steiner
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
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
Carmen Simioni
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Giulia B. Costa
Affiliation:
Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Paulo A. Horta
Affiliation:
Phycology Laboratory, Department of Botany, Federal University of Santa Catarina, 88040-900, Florianópolis, SC, Brazil
Fungyi Chow
Affiliation:
Department of Botany, Institute of Bioscience, University of São Paulo, 05508-090, São Paulo, SP, Brazil
Fernanda Ramlov
Affiliation:
Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, 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:
Central Laboratory of Electron Microscopy, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
Éder C. Schmidt*
Affiliation:
Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88049-900, CP 476, Florianópolis, SC, Brazil
*
*Corresponding author. [email protected]; [email protected]
Get access

Abstract

The in vitro effect of cadmium (Cd) on apical segments of Pterocladiella capillacea was examined. Over a period of 7 days, the segments were cultivated with the combination of different salinities (25, 35, and 45 practical salinity units) and Cd concentrations, ranging from 0.17 to 0.70 ppm. The effects of Cd on growth rates and content of photosynthetic pigments were analyzed. In addition, metabolic profiling was performed, and samples were processed for microscopy. Serious damage to physiological performance and ultrastructure was observed under different combinations of Cd concentrations and salinity values. Elementary infrared spectroscopy revealed toxic effects registered on growth rate, photosynthetic pigments, chloroplast, and mitochondria organization, as well as changes in lipids and carbohydrates. These alterations in physiology and ultrastructure were, however, coupled to activation of such defense mechanisms as cell wall thickness, reduction of photosynthetic harvesting complex, and flavonoid. In conclusion, P. capillacea is especially sensitive to Cd stress when intermediate concentrations of this pollutant are associated with low salinity values. Such conditions resulted in metabolic compromise, reduction of primary productivity, i.e., photosynthesis, and carbohydrate accumulation in the form of starch granules. Taken together, these findings improve our understanding of the potential impact of this metal in the natural environment.

Keywords

Pterocladiella capillaceacadmiumsalinitymorphologymetabolic profilemetal toxicity
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 20 , Issue 5 , October 2014 , pp. 1411 - 1424
Copyright
© Microscopy Society of America 2014 

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.)

References

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
Armisén, R. & Galatas, F. (1987). Production, properties and uses of agar. In Production and Utilization of Products from Commercial Seaweeds, FAO Fishing Technical Paper, McHugh, D.J. (Ed.), pp. 1–57. Rome, Italy: FAO.Google Scholar
Bouzon, Z.L., Ferreira, E.C., Dos 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
Cocchi, M., Foca, G., Lucisano, M., Marchetti, A., Pagani, M.A., Lorenzo, T. & Ulrici, A. (2004). Classification of cereal flours by chemometric analysis of MIR spectra. J Agric Food Chem 52, 1062–1067.CrossRefGoogle ScholarPubMed
Diannelidis, B.E. & Delivopoulos, S.G. (1997). The effects of zinc, copper and cadmium on the fine structure of Ceramium ciliatum (Rhodophyceae, Ceramiales). Mar Environ Res 44, 127–134.CrossRefGoogle Scholar
Edwards, P. (1970). Illustrated guide to the seaweeds and sea grasses in the vicinity of Port Aransas. Texas Contr Mar Sci 15, 1–228.Google Scholar
Ferreira, D., Barros, A., Coimbra, M.A. & Delgadillo, I. (2001). Use of FT-IR spectroscopy to follow the effect of processing in cell wall polysaccharide extracts of a sun-dried pear. Carbohydr Polymers 45, 175–182.CrossRefGoogle Scholar
Fritioff, A., Kautsky, L. & Greger, M. (2005). Influence of temperature and salinity on heavy metal uptake by submersed plants. Environ Pollut 133, 265–274.CrossRefGoogle ScholarPubMed
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
Intergovernmental Panel on Climate Change (IPCC) (2013). Climate Change 2013: The Physical Science Basis. IPCC Working Group I Contribution to AR5. WHO and UNEP, (IPCC), Stockholm, Sweden. 1535 pp.Google Scholar
Jiang, H.-P., Gao, B.-B., Li, W.-H., Zhu, M., Zheng, C.-F., Zheng, Q.-S. & Wnag, C.-H. (2013). Physiological and biochemical responses of Ulva prolifera and Ulva linza to cadmium stress. Sci World J 2013, 1–11.Google ScholarPubMed
Kakinuma, M., Coury, D.A., Kuno, Y., Itoh, S., Kozawa, Y., Inagaki, E., Yoshiura, Y. & Amano, H. (2006). Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Mar Biol 149, 97–106.CrossRefGoogle Scholar
Katz, S., Kizner, Z., Dubinsky, Z. & Friedlander, M. (2000). Responses of Porphyra linearis (Rhodophyta) to environmental factors under controlled culture conditions. J Appl Phycol 12, 535–542.CrossRefGoogle Scholar
Kuhnen, S., Ogliari, J.B., Dias, P.F., Boffo, E.F., Correia, I., Ferreira, A.G., Delgadillo, I. & Maraschin, M. (2010). ATR-FTIR spectroscopy and chemometric analysis applied to discrimination of landrace maize flours produced in southern Brazil. Food Sci Technol 45, 1673–1681.Google Scholar
Kumar, M., Kumari, P., Gupta, V., Reddy, C.R.K. & Jha, B. (2010). Biochemical responses of red alga Gracilaria corticata (Gracilariales, Rhodophyta) to salinity induced oxidative stress. J Exp Mar Biol Ecol 391, 27–34.CrossRefGoogle Scholar
Kursar, T.A., Van Der Meer, J. & Alberte, R.S. (1983). Light-harvesting system of the red alga Gracilaria tikvahiae: I. Biochemical analyses of pigment mutations. Plant Physiol 73, 353–360.CrossRefGoogle ScholarPubMed
Lambert, J.B., Shurvell, H.F., Lightner, D.A. & Cooks, R.G. (2001). Organic Structural Spectroscopy. Upper Saddle River: Prentice Hall. 568 pp.Google Scholar
Lignell, A. & Pedersén, M. (1989). Agar composition as a function of morphology and growth rate. Studies on some morphological strains of Gracilaria secundata and Gracilaria verrucosa (Rhodophyta). Bot Mar 32, 219–227.CrossRefGoogle Scholar
Mamboya, F., Lyimo, T.J., Landberg, T. & Björk, M. (2009). Influence of combined changes in salinity and copper modulation on growth and copper uptake in the tropical green macroalga Ulva reticulata. Estuar, Coas Shelf Sci 84, 326–330.CrossRefGoogle 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 macroalga Padina boergensenii. In Proceedings of the Conference on Advances on Marine Sciences in Tanzania, Richmond, M.D. & Francis, J. (Eds.), pp. 185–192. Tanzania: Bilateral Marine Science Programme.Google Scholar
Mamboya, F.A., Pratap, H.B., Mtolera, M. & Björk, M. (2007). Accumulation of copper and zinc and their effects on growth and maximum quantum yield of the brown macroalga Padina gymnospora. West Indian Ocean J Mar Sci 6, 17–28.Google Scholar
Martins, C.D.L., Arantes, N., Faveri, C., Batista, M.B., Oliveira, E.C., Pagliosa, P.R., Fonseca, A.L., Nunes, J.M.C., Chow, F., Pereira, S.B. & Horta, P.A. (2012). The impact of coastal urbanization on the structure of phytobenthic communities in southern Brazil. Mar Pollut Bull 64, 772–778.CrossRefGoogle ScholarPubMed
Millan-Testa, C.E., Mendez-Montealvo, M.G., Ottenhof, M.A., Farhat, I.A. & Bello-Pérez, L.A. (2005). Determination of the molecular and structural characteristics of okenia, mango and banana starches. J Agric Food Chem 53, 495–501.CrossRefGoogle ScholarPubMed
Oh, J.-J, Choi, E.-M, Han, Y.-S, Yoon, J.-H, Park, A, Jin, K, Lee, J.-W., Choi, H., Kim, S., Brown, M.T. & Han, T. (2012). Influence of Salinity on Metal Toxicity to Ulva pertusa. Toxicology and Environmental Health Sciences 4, 9–13.CrossRefGoogle Scholar
Oliveira, E.C. & Berchez, F.A.S. (1993). Resource biology of Pterocladia capillacea (Gelidiales, Rhodophyta) populations in Brazil. Hydrobiologia 260, 255–261.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
Santos, R.W., Schmidt, E.C., & Bouzon, Z.L. (2013). Changes in ultrastructure and cytochemistry of the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales) treated with cadmium. Protoplasma 250, 297–305.CrossRefGoogle ScholarPubMed
Scherner, F., Horta, P.A., Oliveira, E.C., Simonassi, J.C., Hall-Spencer, J.M., Chow, F., Nunes, J.M.C. & Pereira, S.M.B. (2013). Coastal urbanization leads to remarkable seaweed species loss and community shifts along the SW Atlantic. Mar Pollut Bull 76, 106–115.CrossRefGoogle ScholarPubMed
Scherner, F., Ventura, R., Barufi, J.B. & Horta, P.A. (2012 a). Salinity critical threshold values for photosynthesis of two cosmopolitan seaweed species: Providing baselines for potential shifts on seaweed assemblages. Mar Environ Res 79, 1–12.Google Scholar
Scherner, F., Barufi, J.B. & Horta, P.A. (2012 b). Photosynthetic response of two seaweed species along an urban pollution gradient: Evidence of selection of pollution-tolerant species. Mar Pollut Bull 64, 2380–2390.CrossRefGoogle ScholarPubMed
Schmidt, E.C., Maraschin, M. & Bouzon, Z.L. (2010 a). 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. (2010 b). 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., PaulaM., R., Latini, A., Maraschin, M. & Bouzon, Z.L. (2012). 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., 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
Schulz, H. & Baranska, M. (2007). Identification and qualitification of valuable plant substances by IR and Raman spectroscopy. Vib Spectrosc 43, 13–25.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. (2002). Fine structure and X-ray microanalysis of a red macrophyte cultured under cadmium stress. Environ Pollut 120, 813–821.CrossRefGoogle ScholarPubMed
Toledo, F.A.L., Costa, K.B. & Pivel, M.A.G. (2007). Salinity changes in the western tropical South Atlantic during the last 30 kyr. Global Planet Change 57, 383–395.CrossRefGoogle Scholar
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. Braz J Pharmacog 21, 355–360.CrossRefGoogle Scholar
Wang, W.X. & Dei, R.C.H. (1999). Kinetic measurements of metal accumulation in two marine macroalgae. Mar Biol 135, 11–23.CrossRefGoogle Scholar
Wellburn, A.R. (1994). 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
Wernberg, T., Smale, D.A., Tuya, F., Thomsen, M.S., Langlois, T.J., de Bettignies, T., Bennett, S. & Rousseaux, C.S. (2013). An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3, 78–82.CrossRefGoogle Scholar
Yokoya, N.S. & Oliveira, E.C. (1992). Effects of salinity on the growth rate, morphology and water content of some Brazilian red algae of economic importance. Cienc Mar, México 18, 49–64.CrossRefGoogle Scholar
Zacarias, A.A., Moresco, H.H., Horst, H., Brighente, I.M.C., Marques, M.C.A. & Pizzollati, M.G. (2007). Determinação do teor de fenólicos e flavonóides no extrato e frações de Tabebuia heptaphylla. 30a Reunião Anual da Sociedade Brasileira de Química, Santa Maria, Rio Grande do Sul.Google Scholar