Abstract
Sulphate is an essential nutrient for autotrophic organisms and has been shown to have important implications in certain processes of tolerance to cadmium toxicity. Sodium sulphate is the main salt of sulphate in the natural environments. The concentration of this salt is increasing in the aquatic environments due to environmental pollution. The aim of this study was to investigate, using an analysis of isobolograms, the type and the degree of the interaction between Cd(II) and sodium sulphate in the freshwater microalga Chlamydomonas moewusii. Two blocks of experiments were performed, one at sub-optimal sodium sulphate concentrations (<14.2 mg/L) and the other at supra-optimal concentrations (>14.2 mg/L). Three fixed ratios (2:1, 1:1, and 1:2) of the individual EC50 for cadmium and sodium sulphate were used within each block. The isobolographic analysis of interaction at sub-optimal concentrations showed a stronger antagonistic effect with values of interaction index (γ) between 1.46 and 3.4. However, the isobologram with sodium sulphate at supra-optimal concentrations revealed a slight but significant synergistic effect between both chemicals with an interaction index between 0.54 and 0.64. This synergic effect resulted in the potentiation of the toxic effects of cadmium, synergy that was related to the increase of the ionic strength and of two species of cadmium, CdSO4 (aq), and Cd(SO4) 2 −2 , in the medium. Results of the current study suggest that sodium sulphate is able to perform a dual antagonist/synergist effect on cadmium toxicity. This role was concentration dependent.
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Ahmad A, Abdin MZ (2000) Photosynthesis and its related physiological variables in the leaves of Brassica genotypes as influenced by sulphur fertilization. Physiol Plantarum 110:144–149
Alves de Oliveira J, Cambraia J, Valle de Sousa M, Oliva MA (2009) Sulphate uptake and metabolism in water hyacinth and salvinia during cadmium stress. Aquat Bot 91:257–261
Anjum NA, Umar S, Ahmad A, Iqbal M, Khan NA (2008) Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regul 54:271–279
Baścik-Remisiewicz A, Aksmann A, Żak A, Kowalska M, Tukaj Z (2011) Toxicity of cadmium, anthracene, and their mixture to Desmodesmus subspicatus estimated by algal growth-inhibition ISO standard test. Arch Environ Contam Toxicol 60:610–617
Bochenek M, Etherington GJ, Koprivova A, Mugford ST, Bell TG, Malin G, Kopriva S (2013) Transcriptome analysis of the sulfate deficiency response in the marine microalga Emiliania huxleyi. New Phytol 199:650–662
Bowell RJ (2000) Sulphate and salt minerals: the problem of treating mine waste. Min Environ Manage 5:11–13
Carfagna S, Salbitani G, Vona V, Esposito S (2011) Changes in cysteine and O-acetyl-l-serine levels in the microalga Chlorella sorokiniana in response to the S-nutritional status. J Plant Physiol 168:2188–2195
Cataldo DA, Garland TR, Wildung RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848
Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832
Davies TD (2007) Sulphate toxicity to the aquatic moss, Fontinalis antipyretica. Chemosphere 66:444–451
Ernst WHO, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143
Filek M, Keskinen R, Hartikainen H, Szarejko I, Janiak A, Miszalski Z, Golda A (2008) The protective role of selenium in rape seedlings subjected to cadmium stress. J Plant Physiol 165:833–844
Folgar S, Torres E, Pérez-Rama M, Cid A, Herrero C, Abalde J (2009) Dunaliella salina as a marine microalga highly tolerant to but a poor remover of cadmium. J Hazard Mater 165:486–493
García-García JD, Olin-Sandoval V, Saavedra E, Girard L, Hernández G, Moreno-Sánchez R (2012) Sulfate uptake in photosynthetic Euglena gracilis. Mechanisms of regulation and contribution to cysteine homeostasis. BBA-Gen Subects 1820:1567–1575
Gessner PK (1995) Isobolographic analysis of interactions: an update on applications and utility. Toxicology 105:161–179
Gessner PK, Cabana BE (1970) A study of the interaction of the hypnotic effects and of the toxic effects of chloral hydrate and ethanol. J Pharmacol Exp Ther 174:247–259
Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants: probing the role of sulfur. Plant Signal Behav 6:215–222
Giordano M, Norici A, Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166:371–382
González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22:2058–2084
Grill E, Winnacker EL, Zenk MH (1987) Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci U S A 84:439–443
Gustafsson JP (2013) Visual MINTEQ version 3.1 [online]. Department of Land and Water Resources Engineering. Royal Intitute of Technology, Stockholm
Hamdy AA (2000) Biosorption of heavy metals by marine algae. Curr Microbiol 41:232–238
Hasanuzzaman M, Fujita M (2013) Cadmium: characteristics, sources of exposure, health and environmental effects. In: Hasanuzzaman M, Fujita M (eds) Chemistry Research and Applications. Nova Publishers, New York, p 369
Holmer M, Storkholm P (2001) Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwater Biol 46:431–451
Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Botany 2012:1–37
Järup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208
Källqvist T (2009) Effect of water hardness on the toxicity of cadmium to the green alga Pseudokirchneriella subcapitata in an artificial growth medium and nutrient-spiked natural lake waters. J Toxicol Environ Health A 72:277–283
Langston WJ (1990) Toxic effects of metals and the incidence of metal pollution in marine ecosystems. In: Furness RW, Rainbow PS (eds) Heavy Metals in the Marine Environment. CRC Press, Boca Raton, Florida, pp 101–122
Lavoie M, Campbell PG, Fortin C (2012) Extending the biotic ligand model to account for positive and negative feedback interactions between cadmium and zinc in a freshwater alga. Environ Sci Technol 46:12129–12136
Loewe S (1927) Die mischiarnei. Klin Wochenschr 6:1077–1085
Lopez-Chuken UJ, Young SD (2010) Modelling sulphate-enhanced cadmium uptake by Zea mays from nutrient solution under conditions of constant free Cd2+ ion activity. J Environ Sci 22:1080–1085
Ma N, Li C, Dong X, Wang D, Xu Y (2015) Different effects of sodium chloride preincubation on cadmium tolerance of Pichia kudriavzevii and Saccharomyces cerevisiae. J Basic Microbiol 55:1002–12
Mariem W, Kilani BR, Benet G, Abdelbasset L, Stanley L, Charlotte P, Chedly A, Tahar G (2014) How does NaCl improve tolerance to cadmium in the halophyte Sesuvium portulacastrum? Chemosphere 117:243–50
Marino R, Howarth RW, Chan F, Cole JJ, Likens GE (2003) Sulfate inhibition of molybdenum-dependent nitrogen fixation by planktonic cyanobacteria under seawater conditions: a non-reversible effect. Hydrobiologia 500:277–293
Mason CF (2002) Biology of freshwater pollution. Pearson Education Limited, Harlow
McLaughlin MJ, Andrew SJ, Smart MK, Smolders E (1998) Effects of sulfate on cadmium uptake by Swiss chard: I. Effects of complexation and calcium competition in nutrient solutions. Plant Soil 202:211–216
Mei X, Li S, Li Q, Yang Y, Luo X, He B, Li H, Xu Z (2014) Sodium chloride salinity reduces Cd uptake by edible amaranth (Amaranthus mangostanus L.) via competition for Ca channels. Ecotoxicol Environ Saf 105:59–64
Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671
Mera R, Torres E, Abalde J (2014) Sulphate, more than a nutrient, protects the microalga Chlamydomonas moewusii from cadmium toxicity. Aquat Toxicol 148C:92–103
Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37
Mislin H, Ravera O (1986) Cadmium in the environment. Experientia Supplementum, 50. Birkhäuser Verlag Basel, Basel
Nazar R, Iqbal N, Masood A, Khan MIR, Syeed S, NA K (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489
Niyogi S, Wood CM (2004) Biotic ligand model, a flexible tool for developing site-specific water quality guidelines for metals. Environ Sci Technol 38:6177–6192
Nocito FF, Pirovano L, Cocucci M, Sacchi GA (2002) Cadmium-induced sulfate uptake in maize roots. Plant Physiol 129:1872–1879
Nocito FF, Lancilli C, Crema B, Fourcoy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148
Pérez-Rama M, Torres E, Abalde J (2006) Composition and production of thiol constituents induced by cadmium in the marine microalga Tetraselmis suecica. Environ Toxicol Chem 25:128–136
Radway JC, Wilde EW, Whitaker MJ, Weissman JC (2001) Screening of algal strains for metal removal capabilities. J Appl Phycol 13:451–455
Rai LC, Gaur JP, Kumar HD (1981) Phycology and heavy-metal pollution. Biol Rev 56:99–151
Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotech 8:221–226
Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ 20:600–608
Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Shafi M, Bakht J, Hassan MJ, Raziuddin M, Zhang G (2009) Effect of cadmium and salinity stresses on growth and antioxidant enzyme activities of wheat (Triticum aestivum L.). Bull Environ Contam Toxicol 82:772–776
Suárez C, Torres E, Pérez-Rama M, Herrero C, Abalde J (2010) Cadmium toxicity on the freshwater microalga Chlamydomonas moewusii Gerloff: biosythesis of thiol compounds. Environ Toxicol Chem 29:1–7
Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol 22:19–25
Tallarida RJ (1992) Statistical analysis of drug combinations for synergism. Pain 49:93–97
Tallarida RJ, Porreca F, Cowan A (1989) Statistical analysis of drug-drug and site-site interactions with isobolograms. Life Sci 45:947–961
Torres E, Cid A, Herrero C, Abalde J (1998) Removal of cadmium ions by the marine diatom Phaeodactylum tricornutum Bohlin accumulation and long-term kinetics of uptake. Bioresour Technol 63:213–220
Torres E, Cid A, Herrero C, Abalde J (2000) Effect of cadmium on growth, ATP content, carbon fixation and ultrastructure in the marine diatom Phaeodactylum tricornutum Bohlin. Water Air Soil Pollut 117:1–14
Torres E, Mera R, Abalde J (2013) Toxicity and tolerance in microalgal cells exposed to cadmium: a current overview. In: Hasanuzzaman M, Fujita M (eds) Cadmium: characteristics, sources of exposure, health and environmental effects. Chemistry Research and Applications. Nova Publishers, New York, pp 171–196
Travieso L, Cañizares RO, Borja R, Benitez F, Domínguez AR, Dupeyron R, Valiente V (1999) Heavy metal removal by microalgae. Bull Environ Contam Toxicol 62:144–151
Van Assche F (1998) The relative contributions of different environmental sources to human exposure and the EU cadmium risk assessment, 8th International Nickel Cadmium Conference, Prague
Vatamaniuk OK, Mari S, Lu Y, Rea PA (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. J Biol Chem 275:31451–31459
Veltman K, Huijbregts MA, Hendriks AJ (2010) Integration of biotic ligand models (BLM) and bioaccumulation kinetics into a mechanistic framework for metal uptake in aquatic organisms. Environ Sci Technol 44:5022–5028
Wang QC, Song H (2009) Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Rep 28:1341–1349
Zembala M, Filek M, Walas S, Mrowiec H, Kornaś A, Miszalski Z, Hartikainen H (2010) Effect of selenium on macro- and microelement distribution and physiological parameters of rape and wheat seedlings exposed to cadmium stress. Plant Soil 329:457–468
Zhang BL, Shang SH, Zhang HT, Jabeen Z, Zhang GP (2013) Sodium chloride enhances cadmium tolerance through reducing cadmium accumulation and increasing anti-oxidative enzyme activity in tobacco. Environ Toxicol Chem 32:1420–5
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Mera, R., Torres, E. & Abalde, J. Isobolographic analysis of the interaction between cadmium (II) and sodium sulphate: toxicological consequences. Environ Sci Pollut Res 23, 2264–2278 (2016). https://doi.org/10.1007/s11356-015-5909-1
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DOI: https://doi.org/10.1007/s11356-015-5909-1