Biochemical and morphological responses to cadmium-induced oxidative stress in Cladophora glomerata

This study aimed to assess the effect of cadmium Cd2+ concentrations on biovolume, pigments, malondialdehyde MDA , hydrogen peroxide, proline, total phenolic compounds, total protein, and total carbohydrate contents of Cladophora glomerata . Cultivations of the alga 8.0 ± 0.1 g as fresh weight were exposed to 7.5, 15, 30, and 60 mg/L of Cd2+ ions in 500 mL flasks containing 400 mL of the medium on a shaker at 120 rpm for 7 days. Results of Fourier transform infrared analyses indicated that the amide, anionic, and amino groups had significant rolesin the binding of Cd2+ on C. glomerata. The detrimental effects of the Cd2+ dose not only observed the morphology of the algal cell but also changed the biochemical compounds of C. glomerata. Growth gradually decreased when the alga was exposed to Cd2+ at 15 and 60 mg/L in comparison with the control. High Cd2+ ions concentrations decreased in chlorophyll-a from 14.27 mg/g in control to 9.97 mg/g at 60 mg/L Cd and protein content from 43.60 mg/g in control to 21.66 mg/g at 60 mg/L Cd in the treated cells compared to the control group, whereas they increased stress molecules e.g., MDA and proline as biomarkers in the response mechanisms of algae to Cd2+ exposure. Results indicated that this alga had wide tolerance to high cadmium concentrations, and the stress compounds in the alga with exposure of Cd2+ seemed to be parameters as a biomarker for metal-induced oxidative stress.

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  • Andosch A, Affenzeller MJ, Lütz C, Lütz-Meindl U (2012). A freshwater green alga under cadmium stress: ameliorating calcium effects on ultrastructure and photosynthesis in the unicellular model Micrasterias. Journal of Plant Physiology 169 (15): 1489-1500.
  • Arief VO, Trilestari K, Sunarso J, Indraswati N, Ismadji S (2008). Recent progress on biosorption of heavy metals from liquids using low cost biosorbents: characterization, biosorption parameters and mechanism studies. Clean 36 (12): 937-962.
  • Bates L, Waldren R, Teare I (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39 (1): 205-207.
  • Bellinger E, Sigee D (2010). Introduction to Freshwater Algae. Freshwater Algae: Identification and Use As Bioindicators. Oxford, UK: John Wiley & Sons.
  • Boughalleb F, Abdellaouı R, Mahmoudi M, Bakhshandeh E (2020). Changes in phenolic profile, soluble sugar, proline, and antioxidant enzyme activities of Polygonum equisetiforme in response to salinity. Turkish Journal of Botany 44: 25-35.
  • Branco D, Lima A, Almeida SF, Figueira E (2010). Sensitivity of biochemical markers to evaluate cadmium stress in the freshwater diatom Nitzschia palea (Kützing) W. Smith. AquaticToxicology 99 (2):109-117.
  • Cao DJ, Xie PP, Deng JW, Zhang HM, Ma RX et al. (2015). Effects of Cu2+ and Zn2+ on growth and physiological characteristics of green algae, Cladophora. Environmental Science and Pollution Research 22 (21): 16535-16541.
  • Chen H, Chen J, Guo Y, Wen Y, Liu J et al. (2012). Evaluation of the role of the glutathione redox cycle in Cu (II) toxicity to green algae by a chiral perturbation approach. AquaticToxicology 120:19-26.
  • Choudhary M, Jetley UK, Khan MA, Zutshi S, Fatma T (2007). Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotoxicology and Environmental Safety 66 (2): 204-209.
  • Çelekli A, Gültekin E, Bozkurt H (2016). Morphological and biochemical responses of Spirogyra setiformis exposed to cadmium. Clean 44 (3): 256-262.
  • Çelekli A, Kapı E, Soysal Ç, Arslanargun H, Bozkurt H (2017). Evaluating biochemical response of filamentous algae integrated with different water bodies. Ecotoxicology and Environmental Safety 142: 171-180.
  • Çelekli A, Kapı M, Bozkurt H (2013). Effect of cadmium on biomass, pigmentation, malondialdehyde, and proline of Scenedesmus quadricauda var. longispina. Bulletin of Environmental Contamination and Toxicology 91 (5): 571-576.
  • Dubois M, Gilles KA, Hamilton JK, Rebers Pt, Smith F (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28 (3): 350-356.
  • Ellman GL (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82 (1): 70-77.
  • Gomes PI, Asaeda T (2013). Phytoremediation of heavy metals by calcifying macro-algae (Nitella pseudoflabellata): implications of redox insensitive end products. Chemosphere 92 (10):1328- 1334.
  • Hayat MT, Nauman M, Nazir N, Ali S, Bangash N (2019).
  • Environmental hazards of cadmium: past, present, and future. In:Hasanuzzaman, M, Prasad, M, Fujita, M. (editors).
  • Cadmium Toxicity and Tolerance in Plants. Amsterdam, Netherlands: Elsevier, pp 163-183.
  • Higgins SN, Malkin SY, Todd Howell E, Guildford SJ, Campbell L et al. (2008). An ecological review of Cladophora glomerata (Chlorophyta) in the Laurentian Great Lakes 1. Journal of Phycology 44 (4): 839-854.
  • Jiang HP, Gao BB, Li WH, Zhu M, Zheng CF et al. (2013). Physiological and biochemical responses of Ulva prolifera and Ulva linza to cadmium stress. Scientific World Journal 2013: 1-11.
  • John DM, BA Whitton, JA Brook (2002). The Freshwater Algal Flora of the British Isles. 1st edition. Cambridge, UK: Cambridge University Press.
  • 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 Science 178 (3):307-311.
  • Küpper H, Šetlík I, Šetliková E, Ferimazova N, Spiller M et al. (2003). Copper-induced inhibition of photosynthesis: limiting steps of in vivo copper chlorophyll formation in Scenedesmus quadricauda. Functional Plant Biology 30 (12): 1187-1196.
  • Lane TW, Saito MA, George GN, Pickering IJ, Prince R et al. (2005). Biochemistry: a cadmium enzyme from a marine diatom. Nature 435 (7038): 42.
  • Li H, Yang Z, Dai M, Diao X, Dai S et al. (2019). Input of Cd from agriculture phosphate fertilizer application in China during 2006–2016. The Science of the Total Environment 698: 134- 149.
  • Li S, Ji X, Zhu J, Li C, Jian Y et al. (2019). Utilizing algae for agricultural non-point source pollution control: a review. Journal of AgroEnvironment Science 38 (5): 970-979.
  • Li X, Ping X, Xiumei S, Zhenbin W, Liqiang X (2005). Toxicity of cypermethrin on growth, pigments, and superoxide dismutase of Scenedesmus obliquus. Ecotoxicology and Environmental Safety 60 (2): 188-192.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry193: 265-275.
  • Macfie S, Welbourn P (2000). The cell wall as a barrier to uptake of metal ions in the unicellular green alga Chlamydomonas reinhardtii (Chlorophyceae). Archives of Environmental Contamination and Toxicology 39 (4): 413-419.
  • McCready R, Guggolz J, Silviera V, Owens H (1950). Determination of starch and amylose in vegetables. Analytical Chemistry 22 (9): 1156-1158.
  • Ozturk S, Aslim B, Suludere Z (2010). Cadmium (II) sequestration characteristics by two isolates of Synechocystis sp. in terms of exopolysaccharide (EPS) production and monomer composition. BioresourceTechnology 101 (24): 9742-9748.
  • Paquet N, Lavoie M, Maloney F, Duval JF, Campbell PG et al. (2015).
  • Cadmium accumulation and toxicity in the unicellular alga Pseudokirchneriella subcapitata: Influence of metal-binding exudates and exposure time. EnvironmentalToxicologyand Chemistry 34 (7):1524-1532.
  • Peña-Castro JM, Martínez-Jerónimo F, Esparza-García F, CañizaresVillanueva RO (2004). Phenotypic plasticity in Scenedesmus incrassatulus (Chlorophyceae) in response to heavy metals stress. Chemosphere 57 (11): 1629-1636.
  • Perales-Vela HV, González-Moreno S, Montes-Horcasitas C, Cañizares-Villanueva RO (2007). Growth, photosynthetic and respiratory responses to sub-lethal copper concentrations in Scenedesmus incrassatulus (Chlorophyceae). Chemosphere 67 (11): 2274-2281
  • Perreault F, Oukarroum A, Melegari SP, Matias WG, Popovic R (2012). Polymer coating of copper oxide nanoparticles increases nanoparticles uptake and toxicity in the green alga Chlamydomonas reinhardtii. Chemosphere 87 (11): 1388-1394.
  • Pinto E, Sigaud-Kutner TC, Leitao MA, Okamoto OK, Morse D et al. (2003). Heavy metal–induced oxidative stress in algae 1. Journal of Phycology 39 (6): 1008-1018.
  • Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka E, GodlewskaŻyłkiewicz B (2012). Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiology and Biochemistry 52: 52- 65.
  • Rai U, Singh N, Upadhyay A, Verma S (2013). Chromate tolerance and accumulation in Chlorella vulgaris L.: role of antioxidant enzymes and biochemical changes in detoxification of metals. Bioresource Technology 136: 604-609.
  • Ratkevicius N, Correa J, Moenne A (2003). Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev.(Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell& Environment 26 (10): 1599-1608.
  • Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002). Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24 (5): 417-428.
  • Rıffat A, Ahmad MSA (2020). Regulation of antioxidant activity in maize (Zea mays L.) by exogenous application of sulfur under saline conditions. Turkish Journal of Botany 44: 62-75.
  • Rybak A, Messyasz B, Łęska B (2012). Freshwater Ulva (Chlorophyta) as a bioaccumulator of selected heavy metals (Cd, Ni and Pb) and alkaline earth metals (Ca and Mg). Chemosphere 89 (9):1066-1076.
  • Salama E, Roh H, Dev S, Khan MA, Abou-Shanab RAI et al. (2019). Algae as a green technology for heavy metals removal from various wastewater. World Journal of Microbiology and Biotechnology 35: 75: 1-19.
  • Saleh B (2015). Physiological response of the green algae Ulva lactuca (Chlorophyta) to heavy metals stress. Journal of Stress Physiology & Biochemistry 11 (3): 38-51.
  • Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA et al. (2017). Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171: 710-721.
  • Sergiev I, Alexieva V, Karanov E (1997). Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus del’Academie Bulgare des Sciences 51 (3): 121-124.
  • Souza VL, de Almeida AAF, Lima SG, Cascardo JCDM, Silva DDC et al. (2011). Morphophysiological responses and programmed cell death induced by cadmium in Genipa americana L.(Rubiaceae). Biometals 24 (1): 59-71.
  • Štork F, Bačkor M, Klejdus B, Hedbavny J, Kováčik J (2013). Changes of metal-induced toxicity by H 2 O 2/NO modulators in Scenedesmus quadricauda (Chlorophyceae). Environmental Science and Pollution Research 20 (8): 5502-5511.
  • Templeton DM, Liu Y (2010). Multiple roles of cadmium in cell death and survival. Chemico-BiologicalInteractions 188 (2): 267-275.
  • Tripathi B, Mehta S, Amar A, Gaur J (2006). Oxidative stress in Scenedesmus sp. during short-and long-term exposure to Cu2+ and Zn2+. Chemosphere 62 (4):538-544.
  • Verbruggen N, Hermans C, Schat H (2009). Mechanisms to cope with arsenic or cadmium excess in plants. Current Opinion in Plant Biology 12 (3): 364-372.
  • Wang J, Chen C (2009). Biosorbents for heavy metals removal and their future. Biotechnology Advances 27 (2): 195-226.
  • Wellburn AR (1994). The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometersof different resolution. Journal of Plant Physiology 144 (3): 307-313.
  • Xu D, Li C, Chen H, Shao B (2013). Cellular response of freshwater green algae to perfluorooctanoic acid toxicity. Ecotoxicology and Environmental Safety 88: 103-107.
  • Yvon-Durocher G, Dossena M, Trimmer M, Woodward G, Allen AP (2015). Temperature and the biogeography of algal stoichiometry. Global Ecolology and Biogeography 24 (5): 562-570.
  • Zeraatkar AK, Ahmadzadeh H, Talebi AF, Moheimani NR, McHenry MP (2016). Potential use of algae for heavy metal bioremediation, a critical review. Journal of Environmental Management 181: 817-831.
  • Zhang W, Zhang M, Lin K, Sun W, Xiong B et al. (2012). Ecotoxicological effect of Carbamazepine on Scenedesmus obliquus and Chlorella pyrenoidosa. Environmental Toxicology and Pharmacology 33 (2): 344-352.
  • Zhou Q (2001). The measurement of malondialdehyde in plants. In: Zhou Q (editor): Methods in Plant Physiology.Beijing, China: China Agricultural Press.