Abstract
The induction of antioxidant response and phenotypic plasticity of Scenedesmus quadricauda after exposure to lead (Pb) (3.6 × 10−8 and 3.6 × 10−7 M) at different nitrogen (N) concentrations (1.8 × 10−4, 1.8 × 10−5, and 1.8 × 10−6 M) was investigated. The growth of the microalga was inhibited with decreasing N and increasing Pb concentrations. N limitation and Pb stress caused a decrease in biomass (cell density, dry weight, and chlorophyll a) production. Superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione S transferase (GST) activities generally increased with N limitation and/or increased Pb stress. CAT and POD activities decreased after 48 h, even though their activities were still higher than in those in the control, while GST and SOD activities increased throughout the N/Pb stress exposure period. The enzyme activities observed in S. quadricauda showed a significant positive correlation with N/Pb stress. These results imply that aquatic biota may suffer differently from Pb toxicity, depending on the amount of nitrogen in the environment.
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References
American Public Health Association APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association/Water Environmental Federation, Washington D.C
Anderson RA, Kawachi M (2005) Traditional microalgae isolation techniques. In: Anderson RA (ed) Algal culturing techniques. Elsevier Academic Press, Amsterdam, pp 83–100
Bajguz A (2010) An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environ Exp Bot 68:175–179
Bajguz A (2011) Suppression of Chlorella vulgaris growth by cadmium, lead, and copper stress and its restoration by endogenous Brassinolide. Arch Environ Contam Toxicol 60:406–416
Bere T, Chia AM, Tundisi JG (2012) Effects of Cr III and Pb on the bioaccumulation and toxicity of Cd in tropical periphyton communities: implications of pulsed metal exposures. Environ Pollut 163:184–191
Beyer J, Jonsson G, Porte C, Krahn MM, Ariese F (2010) Analytical methods for determining metabolites of polycyclic aromatic hydrocarbon (PAH) pollutants in fish bile: a review. Environ Toxicol Pharmacol 30:224–244
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Chem 72:243–254
Carfagna S, Lanza N, Salbitani G, Basile A, Sorbo S, Vona V (2013) Physiological and morphological responses of lead or cadmium exposed Chlorella sorokiniana 211-8 K (Chlorophyceae). Springer Plus 2:147
Chia AM, Musa IR (2014) Effect of indigo dye effluent on the growth, biomass production and phenotypic plasticity of Scenedesmus quadricauda (Chlorococcales). Ann Acad Bras Ciênc 86:419–428
Chia AM, Bako SP, Alonge S, Adamu AK (2011) Green algal interactions with physicochemical parameters of some manmade ponds in Zaria, northern Nigeria. Rev Bras Bot 34:285–295
Chia AM, Lombardi AT, Melao MGG, Parrish CC (2013) Effects of cadmium and nitrogen on lipid composition of Chlorella vulgaris (Trebouxiophyceae). Eur J Phycol 48:1–11
Chia AM, Odoh OA, Ladan Z (2014) The indigo blue dye decolorization potential of immobilized Scenedesmus quadricauda. Water Air Soil Pollut. doi:10.1007/s11270-014-1920-2
Contreras L, Mella D, Moenne A, Correa JA (2009) Differential responses to copper induced oxidative stress in the marine macroalgae Lessonia nigrescens and Scytosiphon lomentaria (Phaeophyceae). Aquat Toxicol 94:94–102
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzyrnatic step in rnercapturic acid formation. J Biol Chem 249:7130–7139
Illman AM, Scragg AH, Shales SW (2000) Increase in Chlorella strains calorific values when grown in low nitrogen medium. Enzyme Microb Technol 27:631–635
Jamers A, Van der Ven K, Moens L, Robbens J, Potters G, Guisez Y, Blust R, De Coen W (2006) Effect of copper exposure on gene expression profiles in Chlamydomonas reinhardtii based on microarray analysis. Aquat Toxicol 80:249–260
Ji Y, Sherrel RM (2008) Differential effects of phosphorus limitation on cellular metals in Chlorella and Microcystis. Limnol Oceanogr 53:1790–1804
Knauert S, Knauer K (2008) The role of reactive oxygen species in copper toxicity to two freshwater green algae. J Phycol 44:311–319
Kováčik J, Klejdus B, Hedbavny J, Bačkor M (2010) Effect of copper and salicylic acid on phenolic metabolites and free amino acids in Scenedesmus quadricauda (Chlorophyceae). Plant Sci 178:307–311
Liu G, Chai X, Shao Y, Hu L, Xie Q, Wu H (2011) Toxicity of copper, lead, and cadmium on the motility of two marine microalgae Isochrysis galbana and Tetraselmis chui. J Environ Sci 23:330–335
Liu ZY, Wang GC, Zhou BC (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722
Lombardi AT, Hidalgo TMDR, Vieira AAH, Sartori AL (2007) Toxicity of ionic copper to the freshwater microalga Scenedesmus acuminatus (Chlorophyceae, Chlorococcales). Phycologia 46:74–78
Luck H (1974) In: Methods in Enzymatic Analysis 2 (ed. Bergmeyer), Academic Press New York
Lukas M, Sperfeld E, Wacker A (2011) Growth rate hypothesis does not apply across colimiting conditions: cholesterol limitation affects phosphorus homeostasis of an aquatic herbivore. Funct Ecol 25:1206–1214
Miller AF (2012) Superoxide dismutases: ancient enzymes and new insights. FEBS Lett 586:585–595
Misra HP, Fridovich I (1972) The generation of superoxide radical antioxidation of haemoglobin. J Biol Chem 247:6960–6962
Mohammed MH, Markert B (2006) Toxicity of heavy metals on Scenedesmus quadricauda (Turp.) de Brébisson in batch cultures. Environ Sci Pollut Res 13:98–104
Monteiro CM, Fonseca SC, Castro PML, Malcata FX (2011) Toxicity of cadmium and zinc on two microalgae, Scenedesmus obliquus and Desmodesmus pleiomorphus, from Northern Portugal. J Appl Phycol 23:97–103
Németh J (1998) A biológiai vízminősítés módszerei. (Methods of biological water quality assessment.) Vízi Természet- és Környezetvédelem sorozat, 7. Bp.: Környezetgazdálkodási Intézet: 1-304
OECD-Organisation for Economic Co-operation and Development (1984) Alga growth inhibition test. OECD Guideline for Testing of Chemicals 201, France
Peña-Castro JM, Martínez-Jerónimo F, Esparza-García F, Cañizares-Villanueva RO (2004) Phenotypic plasticity in Scenedesmus incrassatulus (Chlorophyceae) in response to heavy metals stress. Chemosphere 57:1629–1636
Pickett-Heaps JD (1975) Green algae. Sinauer Associates, Sunderland, MS 606
Pinto E, Sigaud-Kutner TCS, Leaito MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal induced oxidative stresss in algae. J Phycol 39:1008–1018
Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z (2009) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquat Toxicol 94:56–61
Reddy JK, Suga T, Mannaerts GP, Lazarow PB, Subramani S (eds) (1995) Peroxisomes: biology and role in toxicology and disease. New York: Ann N Y Acad Sci 804:1–795
Reynolds CS (2006) Ecology of phytoplankton. Cambridge University Press, Cambridge
Sabatini SE, Juarez AB, Eppis MR, Bianchi L, Luquet CM, de Molina MDR (2009) Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicol Environ Saf 72:1200–1206
Salinas AE, Wong MG (1999) Glutathione S-transferases - a review. Curr Med Chem 6: 279–309.
Scarano G, Morelli G (2002) Characterization of cadmium- and lead-phytochelatin complexes formed in a marine microalga in response to metal exposure. Biometals 15:145–151
Scheidegger C, Behra R, Sigg L (2011) Phytochelatin formation kinetics and toxic effects in the freshwater alga Chlamydomonas reinhardtii upon short- and long-term exposure to lead (II). Aquat Toxicol 101:423–429
Serra A, Guasch H, Admiraal W, Van Beusekom SAM, Vandar Geest HG (2010) Influence of phosphorus on copper sensitivity of fluvial periphyton: the role of chemical, physiological and community-related factors. Ecotoxicology 19:770–780
Shoaf WT, Lium BW (1976) Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnol Oceanogr 21:926–928
Szivak I, Behra R, Sigg L (2009) Metal-induced reactive oxygen species production in Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 45:427–435
Torres MA, Barros MP, Campos SCG, Pinto E, Rajamani S, Sayre RT, Colepicolo P (2008) Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol Environ Saf 71:1–15
Tripathi BN, Gaur JP (2004) Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397–404
Trzcińska M, Pawlik-Skowrońska B (2013) Differences in Zn and Pb resistance of two ecotypes of the microalga Eustigmatos sp. inhabiting metal loaded calamine mine spoils. J Appl Phycol 25:277–284
United States Environmental Protection Agency – USEPA (2014) Drinking water contaminants. http://water.epa.gov/drink/contaminants/index.cfm. Accessed 27th March 2014
Vestena S, Cambraia J, Ribeiro C, Oliveira JA, Oliva MA (2011) Cadmium-induced oxidative stress and antioxidant enzyme response in water hyacinth and Salvinia. Braz J Plant Physiol 23:131–139
Wang WX, Dei RCH (2001) Effects of major nutrient additions on metal uptake in phytoplankton. Environ Pollut 111:233–240
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. SA J Bot 76:167–179
Yap CK, Ismail A, Omar H, Tan SG (2004) Toxicities and tolerances of Cd, Cu, Pb and Zn in a primary producer (Isochrysis galbana) and in a primary consumer (Perna viridis). Environ Int 29:1097–1104
Zhang W, Xiong B, Chen L, Lin K, Cui X, Bi H, Guo M, Wang W (2013) Toxicity assessment of Chlorella vulgaris and Chlorella protothecoides following exposure to Pb (II). Environ Toxicol Pharmacol 36:51–57
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Chia, M.A., Chimdirim, P.K. & Japhet, W.S. Lead induced antioxidant response and phenotypic plasticity of Scenedesmus quadricauda (Turp.) de Brébisson under different nitrogen concentrations. J Appl Phycol 27, 293–302 (2015). https://doi.org/10.1007/s10811-014-0312-8
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DOI: https://doi.org/10.1007/s10811-014-0312-8