Manganese accumulation and its effects on three tropical aquatic macrophytes: <i>Azolla caroliniana, Salvinia mínima</i> and <i>Spirodela polyrhiza</i>

Lizieri, Claudineia; Aguiar, Rosane; Kuki, Kacilda Naomi

doi:10.1590/S2175-78602011000400016

Abstract

The phytoremediation technique, which consists of using plants to remove ions, has been increasingly chosen over past decades due to its low-cost technology to mitigate contaminated areas. The aim of this study was to evaluate the potential of the aquatic macrophytes, Azolla caroliniana Willd, Salvinia minima Baker and Spirodela polyrhiza (L.) Schleiden, to accumulate manganese (Mn), an element which, at high concentrations, may be toxic to human populations. The three species accumulated Mn in their tissues and the absorption was independent of the metal concentration in the solution. Spirodela polyrhiza accumulated Mn at higher concentrations of the ion (17.062 mg g^-1 MS), followed by S. minima (4.283 mg g^-1 MS) and A. caroliniana (1.341 mg g^-1 MS). Manganese excess reduced total chlorophyll content in all three species. Carotenoid content was reduced in A. caroliniana (27.02 %) and S. polyrhiza (25.34 %). Growth was only significantly reduced (21.34%) in S. polyrhiza. The species A. caroliniana and S. minima were able to tolerate excess Mn, but were inefficient regarding the accumulation of high concentrations of the metal. High accumulated Mn content in the tissues of S. polyrhiza suggests that the species is able to accumulate this element. Therefore, it has potential for use in phytoremediation and provides a new resource for exploring the Mn accumulation mechanism.

Key words:
aquatic plants; growth; toxicity; phytoremediation

Resumo

A fitorremediação que consiste na utilização de plantas para remoção de íons, tem aumentado nas últimas décadas, tendo em vista a busca por tecnologias de baixo custo para mitigar áreas contaminadas. O objetivo do presente trabalho foi avaliar o potencial das macrófitas aquáticas: Azolla caroliniana Willd, Salvinia minima Baker (Salviniaceae) e Spirodela polyrhiza (L.) Schleiden (Araceae) em acumular manganês (Mn), um elemento que em concentração elevada pode ser tóxico para população humana. As três espécies acumularam Mn em seus tecidos e a absorção foi dependente da concentração do metal em solução. Spirodela polyrhiza acumulou as concentrações mais elevadas de Mn (17,062 mg g^-1 MS), seguida por S. minima (4,283 mg g^-1 MS) e A. caroliniana (1,341 mg g^-1 MS). O excesso de Mn causou redução do conteúdo de clorofila total nas três espécies. O conteúdo de carotenóides diminuiu em A. caroliniana (27,02 %) e S. polyrhiza (25,34 %). Apenas em S. polyrhiza o crescimento foi reduzido significativamente (21,34%). As espécies A. caroliniana e S. minima toleraram excessos de Mn, mas foram ineficientes no acúmulo de concentrações elevadas do metal. O elevado conteúdo de Mn acumulado nos tecidos de S. polyrhiza sugere que a espécie possui capacidade para acumular este elemento. Portanto, apresenta potencial para ser utilizada na fitorremediação e oferece um novo recurso para explorar os mecanismos de acúmulo do Mn.

Palavras-chave:
plantas aquáticas; crescimento; toxicidade; fitorremediação

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Texto completo disponível apenas em PDF.

References

Arnon, D.I. 1949. Copper enzymes in isolated chloroplast polyphenol-oxidases in Beta vulgaris Plant Physiology 24: 1-15.
Asrar, Z.; Khavari-Nejad, R.A. & Heidari, H. 2005. Excess manganese effects on pigments of Mentha spicata at flowering stage. Archives of Agronomy and Soil Science 51: 101-107.
Banks, D.; Younger, P.L.; Arnesen, R.T.; Iversen, E.R. & Banks, S.B. 1997. Minewater chemistry: the good, the bad and the ugly. Environmental Geology 32: 157-174.
Barceló, J. & Poschenrieder, C. 1990. Plant water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition 13: 1-37.
Beale, S.I. 1999. Enzymes of chlorophyll biosynthesis. Photosynthesis Research 60: 43-73.
Boucher, A.M. & Watzin, M.C. 1999. Toxicity identification evaluation of metal-contaminated sediments using an artificial pore-water containing dissolved organic carbons. Environmental Toxicology and Chemistry 18: 509-518.
Cabana, G.; Tremblay, A.; Kaff, J. & Rasmussen, J.B. 1994. Pelagic food chain structure in Ontario Lakes: a determinant of mercury levels in lake trout (Salvelinus namaycush). Canadian Journal of Fisheries and Aquatic Sciences 51: 381-389.
Caldwell, C.R. 1998. Effect of elevated manganese on the ultraviolet and blue light-absorbing compounds of cucumber cotyledon and leaf tissues. Journal of Plant Nutrition 21: 435-445.
Csatorday, K.; Gombos, Z. & Szalontai, B. 1984. Mn²⁺ and Co²⁺ toxicity in chlorophyll biosynthesis. Proceedings of the National Academy of Sciences 81: 476-478.
Chaney, R.L.; Li, Y.M.; Brown, S.L.; Homer, F.A.; Malik, M.; Angle, J.S.; Baker, A.J.M.; Reeves, R.D. & Chin, M. 2000. Improving metal hyperaccumulator wild plants to develop commercial phytoextraction systems: approaches and progress. In: Terry, N. & Bañuelos, G.S. (ed.). Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton. Pp.129-158.
CONAMA - Conselho Nacional do Meio Ambiente. Resolução nº 357, de 17 de março de 2005. Disponível em <http://www.crq4.org.br/downloads/resolucao357.pdf>. Acesso em 22 Fev 2009.
» http://www.crq4.org.br/downloads/resolucao357.pdf
Cunningham, S. & Ow, D. W. 1996. Promises and prospects of phytoremediation. Plant Physiology 110: 715-719.
Doyle, C.J.; Pablo, F.; Lim, R.P. & Hyne, R.V. 2003. Assessment of metal toxicity in sediment pore water from lake Macquarie, Australia. Archives of Environmental Contamination and Toxicology 44: 343-350.
Dushenkov, V.; Kumar, P.B.A.N.; Motto, H. & Raskin, I. 1995. Rizofiltration: The use of plants to remove heavy metals from aqueous streams. Environmental Science & Technology 29: 1239-1245.
Fecht-Christoffers, M.M.; Maier, P. & Horst, W.J. 2003. Apoplastic peroxidases and ascorbate are involved in manganese toxicity and tolerance of Vigna unguiculata Physiologia Plantarum 177: 237-244.
Fernando, D.R.; Bakkaus, E.J.; Perrier, N.; Baker, A.J.M.; Woodrow, I.E.; Batianoff, G.N. & Collins, R,N. 2006. Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytologist 171: 751-758.
Guimarães, F.P. 2006. Potencial de macrofilas para remoção de arsênio e atrazine em solução aquosa. Dissertação de Mestrado. Universidade Federal de Viçosa, Viçosa. 71p.
Guimarães-Silva, A.K.; Machado, D.A.; Nalini, H.A. & Lena, J.C. 2007. A qualidade das águas na região dos garimpos de topázio imperial na sub-bacia do rio da Ponte, Ouro Preto-MG. Revista Escola de Minas 60: 603-611.
Hauck, M.; Mulack, C. & Paul, A. 2002. Manganese uptake in the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides Environmental and Experimental Botany 48: 107-117.
Hoagland, D.R. & Arnon, D.I. 1950. The water-culture method for growing plants without soil. Circular 347. California Agricultural Experiment Station, Berkeley. 37p.
Hoffmann, T. & Kutter, C., Santamaría, J. 2004. Capacity of Salvinia minima Baker to tolerate and accumulate As and Pb. Engineering in Life Sciences 4: 61-65.
Hunt, R. 1978. Plant growth analysis. Edward Arnold Publishers, London. 67p.
Lichtenthaler, H.K. 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzimology 148: 350-382.
Lidon, F.C.; Barreiro, M.G. & Ramalho, J.C. 2004. Manganese accumulation in rice: implications for photosynthetic functioning. Journal of Plant Physiology 161: 1235-1244.
Memon, A.R. & Yatazawa, M. 1980. Distribution of manganese in leaf tissues of manganese accumulator: Acanthopanax sciadophylliodes as revealed by electron probe X-ray microanalyzer. Journal of Plant Nutrition 2: 457-476.
Mergler, D.; Huel, G.; Bowler, R.; Iregren, A.; Belanger, S.; Baldwin, M.; Tardif, R.; Smargiassi, A. & Martin, L. 1994. Nervous system dysfunction among workers with long-term exposure to manganese. Environmental Research 64: 151-180.
Miretzky, P.; Saralegui, A. & Cirelli, A.F. 2004. Aquatic macrophytes potential for the simultaneous removal of heavy metals (Buenos Aires, Argentina). Chemosphere 57: 997-1005.
Mukaopadhyay, M.J. & Sharma, A. 1991. Manganese in cell metabolism of higher plants. Botanical Review 51: 117-149.
Noraho, N. & Gaur, J.P. 1996. Cadmium adsorption and intracellular uptake by two macrophytes, Azolla pinnata and Spirodela polyrhiza Archiv für Hydrobiologie 136: 135-144.
Nichols, P.B.; Couch, J.D. & Al Hamdani, S.H. 2000. Selected physiological responses of Salvinia minima to different chromium concentrations. Aquatic Botany 68: 313-319.
Olguín, E.J.; Hernández, E.; Ramos, I. 2002. The effect of both different light conditions and the pH value on the capacity of Salvinia minima Baker for removing cadmium, lead and chromium. Acta Biotechnologica 22: 121-131.
Oliveira, J.A.; Cambraia, J.; Cano, M.A.O. & Jordão, C.P. 2001. Absorção e acúmulo de cádmio e seus efeitos sobre o crescimento relativo de plantas de aguapé e de salvínia. Revista Brasileira de Fisiologia Vegetal 13: 329-341.
Outridge, P.M.; Hutchinson, T.C. 1991. Induction of cadmium tolerance by acclimation transferred between ramets of the clonal fern Salvinia minima Baker. New Phytologist 117: 597-605.
Rai, U.N.; Sinha, S.; Tripathi, R.D. & Chandra, P. 1995. Wastewater treatability potential of some aquatic macrophytes: Removal of heavy metals. Ecological Engineering 5: 5-12.
Raskin, I. & Ensley, B.D. 2000. Phytoremediation of toxic metals: using plants to clean up the environment. John Wiley and Sons, New York. 303p.
Reichman, S.M. 2002. The responses of plants to metal toxicity: a review focusing on copper, manganese and zinc. Australian Minerals and Energy Environment Foundation, Melbourne. Pp. 14-59.
Richter, C. A. & Azevedo Netto, J. M. 1991. Tratamento de água: tecnologia atualizada. Edgard Blücher, São Paulo. 332p.
Santos, G.V. 2006. Crescimento e respostas antioxidantes de macrófitas aquáticas submetidas ao arsênio. Dissertação de Mestrado. Universidade Federal de Viçosa, Viçosa. 45p.
Sisinno, C.L.S. 2003. Disposição em aterros controlados de resíduos sólidos industriais não-inertes: avaliação dos componentes tóxicos e implicações para o ambiente e para a saúde humana. Cadernos de Saúde Pública 19: 369-374.
Sinha, S.; Rai, U.N. & Chandra, P. 1994. Accumulation and toxicity of iron manganese in Spirodela polrrhiza (L.) Schleiden. Environmental Contamination Toxicology 53: 610-617.
Soares, D.C.F.; Oliveira, E.F.; Silva, G.D.F.; Duarte, L.P.; Pott, V.J. & Vieira Filho, S.A. 2008. Salvinia auriculata: Aquatic bioindicator studied by instrumental neutron activation analysis (INAA). Applied Radiation and Isotopes 66: 561-564.
Tavares, T.M. & Caravalho, F.M. 1992. Avaliação de exposição de populações humanas a metais pesados no ambiente: exemplo do Recôncavo Baiano. Química Nova 15: 147-154.
Tedesco, M.J.; Gianello, C.; Bissani, C.A.; Bohnen, H. & Volkweiss, S.J. 1995. Análise de solo, plantas e outros materiais. UFRGS, Porto Alegre. 174p.
Thornton, I. 1995. Metals in the global environment. International Council on Metal and the Evironment, Ottawa. 53p.
Tripathi, R.D. & Chandra, P. 1991. Chromium uptake by Spirodela polyrrhiza (L.) Schleiden in relation to metal chelators and pH. Environmental Contamination and Toxicology 447: 767-769.
Vissottiviseth, P.; Francesconi, B. & Ridokchana, W. 2002. The potencial of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environmental Pollution 118: 453-461.

Publication Dates

Publication in this collection
Oct-Dec 2011

History

Received
26 Apr 2011
Accepted
26 Aug 2011

This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

[1] Arnon, D.I. 1949. Copper enzymes in isolated chloroplast polyphenol-oxidases in Beta vulgaris Plant Physiology 24: 1-15.

[2] Asrar, Z.; Khavari-Nejad, R.A. & Heidari, H. 2005. Excess manganese effects on pigments of Mentha spicata at flowering stage. Archives of Agronomy and Soil Science 51: 101-107.

[3] Banks, D.; Younger, P.L.; Arnesen, R.T.; Iversen, E.R. & Banks, S.B. 1997. Minewater chemistry: the good, the bad and the ugly. Environmental Geology 32: 157-174.

[4] Barceló, J. & Poschenrieder, C. 1990. Plant water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition 13: 1-37.

[5] Beale, S.I. 1999. Enzymes of chlorophyll biosynthesis. Photosynthesis Research 60: 43-73.

[6] Boucher, A.M. & Watzin, M.C. 1999. Toxicity identification evaluation of metal-contaminated sediments using an artificial pore-water containing dissolved organic carbons. Environmental Toxicology and Chemistry 18: 509-518.

[7] Cabana, G.; Tremblay, A.; Kaff, J. & Rasmussen, J.B. 1994. Pelagic food chain structure in Ontario Lakes: a determinant of mercury levels in lake trout (Salvelinus namaycush). Canadian Journal of Fisheries and Aquatic Sciences 51: 381-389.

[8] Caldwell, C.R. 1998. Effect of elevated manganese on the ultraviolet and blue light-absorbing compounds of cucumber cotyledon and leaf tissues. Journal of Plant Nutrition 21: 435-445.

[9] Csatorday, K.; Gombos, Z. & Szalontai, B. 1984. Mn²⁺ and Co²⁺ toxicity in chlorophyll biosynthesis. Proceedings of the National Academy of Sciences 81: 476-478.

[10] Chaney, R.L.; Li, Y.M.; Brown, S.L.; Homer, F.A.; Malik, M.; Angle, J.S.; Baker, A.J.M.; Reeves, R.D. & Chin, M. 2000. Improving metal hyperaccumulator wild plants to develop commercial phytoextraction systems: approaches and progress. In: Terry, N. & Bañuelos, G.S. (ed.). Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton. Pp.129-158.

[11] CONAMA - Conselho Nacional do Meio Ambiente. Resolução nº 357, de 17 de março de 2005. Disponível em <http://www.crq4.org.br/downloads/resolucao357.pdf>. Acesso em 22 Fev 2009.
» http://www.crq4.org.br/downloads/resolucao357.pdf

[12] Cunningham, S. & Ow, D. W. 1996. Promises and prospects of phytoremediation. Plant Physiology 110: 715-719.

[13] Doyle, C.J.; Pablo, F.; Lim, R.P. & Hyne, R.V. 2003. Assessment of metal toxicity in sediment pore water from lake Macquarie, Australia. Archives of Environmental Contamination and Toxicology 44: 343-350.

[14] Dushenkov, V.; Kumar, P.B.A.N.; Motto, H. & Raskin, I. 1995. Rizofiltration: The use of plants to remove heavy metals from aqueous streams. Environmental Science & Technology 29: 1239-1245.

[15] Fecht-Christoffers, M.M.; Maier, P. & Horst, W.J. 2003. Apoplastic peroxidases and ascorbate are involved in manganese toxicity and tolerance of Vigna unguiculata Physiologia Plantarum 177: 237-244.

[16] Fernando, D.R.; Bakkaus, E.J.; Perrier, N.; Baker, A.J.M.; Woodrow, I.E.; Batianoff, G.N. & Collins, R,N. 2006. Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytologist 171: 751-758.

[17] Guimarães, F.P. 2006. Potencial de macrofilas para remoção de arsênio e atrazine em solução aquosa. Dissertação de Mestrado. Universidade Federal de Viçosa, Viçosa. 71p.

[18] Guimarães-Silva, A.K.; Machado, D.A.; Nalini, H.A. & Lena, J.C. 2007. A qualidade das águas na região dos garimpos de topázio imperial na sub-bacia do rio da Ponte, Ouro Preto-MG. Revista Escola de Minas 60: 603-611.

[19] Hauck, M.; Mulack, C. & Paul, A. 2002. Manganese uptake in the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides Environmental and Experimental Botany 48: 107-117.

[20] Hoagland, D.R. & Arnon, D.I. 1950. The water-culture method for growing plants without soil. Circular 347. California Agricultural Experiment Station, Berkeley. 37p.

[21] Hoffmann, T. & Kutter, C., Santamaría, J. 2004. Capacity of Salvinia minima Baker to tolerate and accumulate As and Pb. Engineering in Life Sciences 4: 61-65.

[22] Hunt, R. 1978. Plant growth analysis. Edward Arnold Publishers, London. 67p.

[23] Lichtenthaler, H.K. 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzimology 148: 350-382.

[24] Lidon, F.C.; Barreiro, M.G. & Ramalho, J.C. 2004. Manganese accumulation in rice: implications for photosynthetic functioning. Journal of Plant Physiology 161: 1235-1244.

[25] Memon, A.R. & Yatazawa, M. 1980. Distribution of manganese in leaf tissues of manganese accumulator: Acanthopanax sciadophylliodes as revealed by electron probe X-ray microanalyzer. Journal of Plant Nutrition 2: 457-476.

[26] Mergler, D.; Huel, G.; Bowler, R.; Iregren, A.; Belanger, S.; Baldwin, M.; Tardif, R.; Smargiassi, A. & Martin, L. 1994. Nervous system dysfunction among workers with long-term exposure to manganese. Environmental Research 64: 151-180.

[27] Miretzky, P.; Saralegui, A. & Cirelli, A.F. 2004. Aquatic macrophytes potential for the simultaneous removal of heavy metals (Buenos Aires, Argentina). Chemosphere 57: 997-1005.

[28] Mukaopadhyay, M.J. & Sharma, A. 1991. Manganese in cell metabolism of higher plants. Botanical Review 51: 117-149.

[29] Noraho, N. & Gaur, J.P. 1996. Cadmium adsorption and intracellular uptake by two macrophytes, Azolla pinnata and Spirodela polyrhiza Archiv für Hydrobiologie 136: 135-144.

[30] Nichols, P.B.; Couch, J.D. & Al Hamdani, S.H. 2000. Selected physiological responses of Salvinia minima to different chromium concentrations. Aquatic Botany 68: 313-319.

[31] Olguín, E.J.; Hernández, E.; Ramos, I. 2002. The effect of both different light conditions and the pH value on the capacity of Salvinia minima Baker for removing cadmium, lead and chromium. Acta Biotechnologica 22: 121-131.

[32] Oliveira, J.A.; Cambraia, J.; Cano, M.A.O. & Jordão, C.P. 2001. Absorção e acúmulo de cádmio e seus efeitos sobre o crescimento relativo de plantas de aguapé e de salvínia. Revista Brasileira de Fisiologia Vegetal 13: 329-341.

[33] Outridge, P.M.; Hutchinson, T.C. 1991. Induction of cadmium tolerance by acclimation transferred between ramets of the clonal fern Salvinia minima Baker. New Phytologist 117: 597-605.

[34] Rai, U.N.; Sinha, S.; Tripathi, R.D. & Chandra, P. 1995. Wastewater treatability potential of some aquatic macrophytes: Removal of heavy metals. Ecological Engineering 5: 5-12.

[35] Raskin, I. & Ensley, B.D. 2000. Phytoremediation of toxic metals: using plants to clean up the environment. John Wiley and Sons, New York. 303p.

[36] Reichman, S.M. 2002. The responses of plants to metal toxicity: a review focusing on copper, manganese and zinc. Australian Minerals and Energy Environment Foundation, Melbourne. Pp. 14-59.

[37] Richter, C. A. & Azevedo Netto, J. M. 1991. Tratamento de água: tecnologia atualizada. Edgard Blücher, São Paulo. 332p.

[38] Santos, G.V. 2006. Crescimento e respostas antioxidantes de macrófitas aquáticas submetidas ao arsênio. Dissertação de Mestrado. Universidade Federal de Viçosa, Viçosa. 45p.

[39] Sisinno, C.L.S. 2003. Disposição em aterros controlados de resíduos sólidos industriais não-inertes: avaliação dos componentes tóxicos e implicações para o ambiente e para a saúde humana. Cadernos de Saúde Pública 19: 369-374.

[40] Sinha, S.; Rai, U.N. & Chandra, P. 1994. Accumulation and toxicity of iron manganese in Spirodela polrrhiza (L.) Schleiden. Environmental Contamination Toxicology 53: 610-617.

[41] Soares, D.C.F.; Oliveira, E.F.; Silva, G.D.F.; Duarte, L.P.; Pott, V.J. & Vieira Filho, S.A. 2008. Salvinia auriculata: Aquatic bioindicator studied by instrumental neutron activation analysis (INAA). Applied Radiation and Isotopes 66: 561-564.

[42] Tavares, T.M. & Caravalho, F.M. 1992. Avaliação de exposição de populações humanas a metais pesados no ambiente: exemplo do Recôncavo Baiano. Química Nova 15: 147-154.

[43] Tedesco, M.J.; Gianello, C.; Bissani, C.A.; Bohnen, H. & Volkweiss, S.J. 1995. Análise de solo, plantas e outros materiais. UFRGS, Porto Alegre. 174p.

[44] Thornton, I. 1995. Metals in the global environment. International Council on Metal and the Evironment, Ottawa. 53p.

[45] Tripathi, R.D. & Chandra, P. 1991. Chromium uptake by Spirodela polyrrhiza (L.) Schleiden in relation to metal chelators and pH. Environmental Contamination and Toxicology 447: 767-769.

[46] Vissottiviseth, P.; Francesconi, B. & Ridokchana, W. 2002. The potencial of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environmental Pollution 118: 453-461.

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