Abstract
Microalgae are among the oldest life forms on Earth and over centuries of evolution they have developed adaptive mechanisms that allow them to survive harsh environmental conditions, including exposure to toxic xenobiotics such as heavy metals (HMs). The response of microalgae to HM stress is like that occurring under any other stress conditions; it generally leads to the formation of reactive oxygen species (ROS). An increased ROS level in algal cells causes alterations of various biological functions, primarily lipid peroxidation, protein oxidation, and nucleic acid damage. To cope with these perturbations, microalgae cells employ several self-defense mechanisms based on the action of ROS-scavenging enzymes and non-enzymatic antioxidant systems. The contribution of phytohormones to the management of oxidative stress is also one of the most important mechanisms. Although several studies suggest that microalgae are potential organisms for the phycoremediation of HMs, the mechanisms by which they cope with oxidative stress remain unclear. This review aims to (i) highlight the oxidative stress of HMs on the cells of microalgae, (ii) describe the enzymatic and biochemical mechanisms by which microalgae manage the oxidative stress, and finally (iii) point out the roles of phytohormones in the regulation of oxidative stress caused by HMs.
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References
Abboud P, Wilkinson KJ (2013) Role of metal mixtures (Ca, Cu and Pb) on Cd bioaccumulation and phytochelatin production by Chlamydomonas reinhardtii. Environ Pollut 179:33–38
Ahii M, Teresa A, Grac M, Parrish CC (2015) Combined nitrogen limitation and cadmium stress stimulate total carbohydrates, lipids, protein and amino acid accumulation in Chlorella vulgaris (Trebouxiophyceae). Aquat Toxicol 160:87–95
Ajitha V, Sreevidya CP, Sarasan M, Park JC, Mohandas A, Sarojini I, Singh B, Puthumana J, Lee J (2021) Effects of zinc and mercury on ROS-mediated oxidative stress-induced physiological impairments and antioxidant responses in the microalga Chlorella vulgaris. Environ Sci Pollut Res Int doi: 10.1007/s11356-021-12950-6
Al-Rashed SA, Ibrahim MM, El-Gaaly GA, Al-Shehri S, Mostafa A (2016) Evaluation of radical scavenging system in two microalgae in response to interactive stresses of UV-B radiation and nitrogen starvation. Saudi J Biol Sci 23:706–712
Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019:6730305
Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell 2014: 360438
Baba SP, Bhatnagar A (2018) Role of thiols in oxidative stress. Curr Opin Toxicol 7:133–139
Bajguz A (2019) Brassinosteroids in microalgae: application for growth improvement and protection against abiotic stresses. In: Hayat S, Yusuf M, Bhardwaj R, Bagjuz A (eds) Brassinosteroids: Plant Growth and Development. Springer Nature, Singapore pp 45–58.
Bajguz A (2011) Suppression of Chlorella vulgaris growth by cadmium, lead, and copper stress and its restoration by endogenous brassinolide. Arch Env Contam Toxicol 60:406–416
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 (2002) Brassinosteroids and lead as stimulators of phytochelatins synthesis in Chlorella vulgaris. J Plant Physiol 324:321–324
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194
Brown MR, Miller KA (1992) The ascorbic acid content of eleven species of microalgae used in mariculture. J Appl Phycol 4:205–215
Çelekli A, Kapi M, Bozkurt H (2013) Effect of cadmium on biomass, pigmentation, malondialdehyde, and proline of Scenedesmus quadricauda var. longispina. Bull Environ Contam Toxicol 91:571–576
Cheng J, Qiu H, Chang Z, Jiang Z, Yin W (2016) The effect of cadmium on the growth and antioxidant response for freshwater algae Chlorella vulgaris. Springerplus 5:1–8
Chisla S, Massey V (1989) Mechanisms of flavoprotein-catalyzed reactions. Eur J Biochem 181:1–17
Cirulis JT, Scott JA, Ross GM (2013) Management of oxidative stress by microalgae. Can J Physiol Pharmacol 91:15–21
Dahmen-Ben Moussa I, Athmouni K, Chtourou H, Ayadi H, Sayadi S, Dhouib A (2018) Phycoremediation potential, physiological, and biochemical response of Amphora subtropica and Dunaliella sp. to nickel pollution. J Appl Phycol 30:931–941
Danouche M, El Ghachtouli N, El Arroussi H (2021) Phycoremediation mechanisms of heavy metals using living green microalgae: physicochemical and molecular approaches for enhancing selectivity and removal capacity. Heliyon 7:e07609
Danouche M, El Ghachtouli N, El Baouchi A, El Arroussi H (2020) Heavy metals phycoremediation using tolerant green microalgae: enzymatic and non-enzymatic antioxidant systems for the management of oxidative stress. J Environ Chem Eng 8:104460
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53
Elleuch J, Ben Amor F, Chaaben Z, Frikha F, Michaud P, Fendri I, Abdelkafi S (2021) Zinc biosorption by Dunaliella sp. AL-1: mechanism and effects on cell metabolism. Sci Total Environ 773:145024
Erland LAE, Turi CE, Saxena PK (2019) Serotonin in plants: origin, functions, and implications. In: Pilowsky PM (ed) Serotonin. The mediator that spans evolution. Elsevier, London pp 23–46.
Falkowska M, Pietryczuk A, Piotrowska A, Bajguz A, Grygoruk A, Czerpak R (2011) The effect of gibberellic acid (GA3) on growth, metal biosorption and metabolism of the green algae Chlorella vulgaris (Chlorophyceae) Beijerinck exposed to cadmium and lead stress. Polish J Environ Stud 20:53–59
Forman HJ, Zhang H, Rinna A (2010) Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30:1–12
Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manage 92:407–418
Gauthier MR, Senhorinho GNA, Scott JA (2020) Microalgae under environmental stress as a source of antioxidants. Algal Res 52:102–104
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gómez-Jacinto V, García-Barrera T, Gómez-Ariza JL, Garbayo-Nores I, Vílchez-Lobato C (2015) Elucidation of the defence mechanism in microalgae Chlorella sorokiniana under mercury exposure. Identification of Hg-Phytochelatins. Chem Biol Interact 238:82–90
Hajiboland R (2014) Reactive oxygen species and photosynthesis. In: Ahmad P (ed) Oxidative Damage to Plants. Elsevier, Amsterdam pp 1–63
Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322
Hamed SM, Selim S, Klöck G, AbdElgawad H (2017a) Sensitivity of two green microalgae to copper stress: growth, oxidative and antioxidants analyses. Ecotoxicol Environ Saf 144:19–25
Hamed SM, Zinta G, Klöck G, Asard H, Selim S, AbdElgawad H (2017b) Zinc-induced differential oxidative stress and antioxidant responses in Chlorella sorokiniana and Scenedesmus acuminatus. Ecotoxicol Environ Saf 140:256–263
Harwood JL (1998) Membrane lipids in algae. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis: structure, function and genetics. Kluwer, Dordrecht pp 53–64
Hasanuzzaman M, Bhuyan MHMB, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8:384
Hashtroudi MS, Ghassempour A, Riahi H, Shariatmadari Z, Khanjir M (2013) Endogenous auxins in plant growth-promoting cyanobacteria—Anabaena vaginicola and Nostoc calcicola. J Appl Phycol 25:379–386
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466
Hirata K, Tsujimoto Y, Namba T, Ohta T, Hirayanagi N, Miyasaka H, Zenk MH, Miyamoto K (2001) Strong induction of phytochelatin synthesis by zinc in marine green alga, Dunaliella tertiolecta. J Biosci Bioeng 92:24–29
Huang H, Ullah F, Zhou D, Yi M, Zhao Y, Terzaghi WB (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:800
Janknegt PJ, De Graaff CM, Van de Poll WH, Visser RJ, Rijstenbil JW, Buma AG (2009) Short-term antioxidative responses of 15 microalgae exposed to excessive irradiance including ultraviolet radiation. Eur J Phycol 44:37–41
Jeong Y, Nakamura J, Upton PB, Swenberg JA (2005) Pyrimido [1,2-α]-purin-10(3H)-one, M1G, is less prone to artifact than base oxidation. Nucleic Acids Res 33:6426–6434
Jiang Y, Purchase D, Jones H, Garelick H (2011) Effects of arsenate (As5+) on growth and production of glutathione (GSH) and phytochelatins (PCS) in Chlorella vulgaris. Int J Phytoremediation 13:834–844
Kagan VE (1989) Tocopherol stabilizes membrane against phospholipase A, free fatty acids, and lysophospholipids. Ann N Y Acad Sci 570:121–135
Kobayashi I, Fujiwara S, Saegusa H, Inouhe M, Matsumoto H, Tsuzuki M (2006) Relief of arsenate toxicity by Cd-stimulated phytochelatin synthesis in the green alga Chlamydomonas reinhardtii. Mar Biotechnol 8:94–101
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
Kováčika J, Klejdusb B, Babulad P, Hedbavny J (2017) Ascorbic acid affects short-term response of Scenedesmus quadricauda to cadmium excess. Algal Res 24:354–359
León-Vaz A, León R, Giráldez I, Vega JM, Vigara J (2021) Impact of heavy metals in the microalga Chlorella sorokiniana and assessment of its potential use in cadmium bioremediation. Aquat Toxicol 239:105941
Leong YK, Chang JS (2020) Bioremediation of heavy metals using microalgae: recent advances and mechanisms. Bioresour Technol 303:122886
Li C, Zheng C, Fu H, Zhai S, Hu F, Naveed S, Zhang C, Ge Y (2021) Contrasting detoxification mechanisms of Chlamydomonas reinhardtii under Cd and Pb stress. Chemosphere 274:129771
Li M, Hu C, Zhu Q, Chen L, Kong Z, Liu Z (2006) Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 62:565–572
Mei LI, Qin ZHU, Hu CW, Li CHEN, Liu ZL, Kong ZM (2007) Cobalt and manganese stress in the microalga Pavlova viridis (Prymnesiophyceae): effects on lipid peroxidation and antioxidant enzymes. J Environ Sci 19:1330–1335
Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19:998–1011
Lu J, Ma Y, Xing G, Li W, Kong X, Li J, Wang L, Yuan H, Yang J (2019) Revelation of microalgae’s lipid production and resistance mechanism to ultra-high Cd stress by integrated transcriptome and physiochemical analyses. Environ Pollut 250:186–195
Lu L, Wu Y, Ding H, Zhang W (2015) The combined and second exposure effect of copper(II) and chlortetracycline on fresh water algae, Chlorella pyrenoidosa and Microcystis aeruginosa. Environ Toxicol Pharmacol 40:140–148
Lu M, Gao F, Li C, Yang H (2021) Response of microalgae Chlorella vulgaris to Cr stress and continuous Cr removal in a membrane photobioreactor. Chemosphere 262:128422
Lu Y, Xu J (2015) Phytohormones in microalgae: a new opportunity for microalgal biotechnology? Trends Plant Sci 20:273–282
Luis P, Behnke K, Toepel J, Wilhelm C (2006) Parallel analysis of transcript levels and physiological key parameters allows the identification of stress phase gene markers in Chlamydomonas reinhardtii under copper excess. Plant Cell Environ 29:2043–2054
Ma X, Chen Y, Liu F, Zhang S, Wei Q (2021) Enhanced tolerance and resistance characteristics of Scenedesmus obliquus FACHB-12 with K3 carrier in cadmium polluted water. Algal Res 55:1–10
Maillard P, Thepenier C, Gudin C (1993) Determination of an ethylene biosynthesis pathway in the unicellular green alga, Haematococcus pluvialis. Relationship between growth and ethylene production. J Appl Phycol 5:93–98
Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193
Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Biol 47:127–158
Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Breusegem F Van, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models 61:4197-4220.
Mohy El-Din SM, Abdel-Kareem MS (2020) Effects of copper and cadmium on the protein profile and DNA pattern of marine microalgae Chlorella salina and Nannochloropsis salina. Environ Process 7:189–205
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–483
Morelli E, Scarano G (2004) Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutum. Plant Sci 167:289–296
Movafeghi A, Khataee A, Rezaee A, Kosari-Nasab M, Tarrahi R (2019) Toxicity of cadmium selenide nanoparticles on the green microalga Chlorella vulgaris: inducing antioxidative defense response. Environ Sci Pollut Res 26:36380–36387
Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299
Nguyen HN, Kisiala AB, Emery RJN (2020a) The roles of phytohormones in metal stress regulation in microalgae. J Appl Phycol 32:3817–3829
Nguyen TQ, Sesin V, Kisiala A, Emery RJN (2020b) The role of phytohormones in enhancing metal remediation capacity of algae. Bull Environ Contam Toxicol 105:671–678
Okamoto OK, Pinto E, Latorre LR, Bechara EJH, Colepicolo P (2001) Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Arch Environ Contam Toxicol 40:18–24
Park AK, Kim I-S, Do H, Jeon BW, Lee CW, Roh SJ, Shin SC, Park H, Kim Y-S, Kim Y-H, Yoon H-S, Lee JH, Kim H-W (2016) Structure and catalytic mechanism of monodehydroascorbate reductase, MDHAR, from Oryza sativa L. japonica. Sci Rep 6:33903
Pawlik-Skowrońska B (2002) Correlations between toxic Pb effects and production of Pb-induced thiol peptides in the microalga Stichococcus bacillaris. Environ Pollut 119:119–127
Pérez-Gálvez A, Viera I, Roca M (2020) Carotenoids and chlorophylls as antioxidants. Antioxidants 9:505
Pikula KS, Zakharenko AM, Aruoja V, Golokhvast KS, Tsatsakis AM (2019) Oxidative stress and its biomarkers in microalgal ecotoxicology. Curr Opin Toxicol 13:8–15
Pinto E, Sigaud-Kutner TC, Leitao MA, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018
Piotrowska-Niczyporuk A, Bajguz A (2017) Response and the detoxification strategies of green alga Acutodesmus obliquus (Chlorophyceae) under lead stress. Environ Exp Bot 144:25–36
Piotrowska-Niczyporuk A, Bajguz A, Kotowska U, Zambrzycka-Szelewa E, Sienkiewicz A (2020) Auxins and cytokinins regulate phytohormone homeostasis and thiol-mediated detoxification in the green alga Acutodesmus obliquus exposed to lead stress. Sci Rep 10:10193
Piotrowska-Niczyporuk A, Bajguz A, Talarek M, Bralska M, Zambrzycka E (2015) The effect of lead on the growth, content of primary metabolites, and antioxidant response of green alga Acutodesmus obliquus (Chlorophyceae). Environ Sci Pollut Res 22:19112–19123
Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka-Szelewa E, Bralska M (2018) Exogenously applied auxins and cytokinins ameliorate lead toxicity by inducing antioxidant defence system in green alga Acutodesmus obliquus. Plant Physiol Biochem 132:535–546
Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka E, Godlewska-Zyłkiewicz B (2012) Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol Biochem 52:52–65
Qian H, Chen W, Sheng GD, Xu X, Liu W, Fu Z (2008) Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquat Toxicol 88:301–307
Rai UN, Singh NK, Upadhyay AK, Verma S (2013) Chromate tolerance and accumulation in Chlorella vulgaris L: role of antioxidant enzymes and biochemical changes in detoxification of metals. Bioresour Technol 136:604–609
Rajput VD, Harish SRK, Verma KK, Sharma L, Quiroz-Figueroa FR, Meena M, Gour VS, Minkina T, Sushkova S, Mandzhieva S (2021) Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology (basel) 10:267
Randhawa VK, Zhou F, Jin X, Nalewajko C, Kushner DJ (2001) Role of oxidative stress and thiol antioxidant enzymes in nickel toxicity and resistance in strains of the green alga Scenedesmus acutus f. alternans. Can J Microbiol 47:987–993
Rezayian M, Niknam V, Ebrahimzadeh H (2019) Oxidative damage and antioxidative system in algae. Toxicol Rep 6:1309–1313
Rocchetta I, Mazzuca M, Conforti V, Balzaretti V, de Molina MdCR (2012) Chromium induced stress conditions in heterotrophic and auxotrophic strains of Euglena gracilis. Ecotoxicol Environ Saf 84:147–154
Rocchetta I, Mazzuca M, Conforti V, Ruiz L, Balzaretti V, De Molina MdCR (2006) Effect of chromium on the fatty acid composition of two strains of Euglena gracilis. Environ Pollut 141:353–358
Rodrigo R, Libuy M (2014) Modulation of plant endogenous antioxidant systems by polyphenols. In: Watson RR (ed) Polyphenols in plants: isolation, purification and extract preparation. Elsevier, Amsterdam pp 65–85
Sabatini SE, Juárez ÁB, Eppis MR, Bianchi L, Luquet CM, Ríos de Molina MDC (2009) Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicol Environ Saf 72:1200–1206
Sánchez-Thomas R, Moreno-Sánchez R, García-García JD (2016) Accumulation of zinc protects against cadmium stress in photosynthetic Euglena gracilis. Environ Exp Bot 131:19–31
Shivaji S, Dronamaraju SVL (2019) Scenedesnus rotundus isolated from the petroleum effluent employs alternate mechanisms of tolerance to elevated levels of cadmium and zinc. Sci Rep 9:8485
Singh S, Eapen S, D’Souza SF (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246
Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3:229–235
Strejckova A, Dvorak M, Klejdus B, Krystofova O, Hedbavny J, Adam V, Huska D (2019) The strong reaction of simple phenolic acids during oxidative stress caused by nickel, cadmium and copper in the microalga Scenedesmus quadricauda. N Biotechnol 48:66–75
Suárez C, Torres E, Pérez-Rama M, Herrero C, Abalde J (2010) Cadmium toxicity on the freshwater microalga Chlamydomonas moewusii Gerloff: biosynthesis of thiol compounds. Environ Toxicol Chem 29:2009–2015
Suman TY, Radhika Rajasree SR, Kirubagaran R (2015) Evaluation of zinc oxide nanoparticles toxicity on marine algae Chlorella vulgaris through flow cytometric, cytotoxicity and oxidative stress analysis. Ecotoxicol Environ Saf 113:23–30
Talarek-Karwel M, Bajguz A, Piotrowska-Niczyporuk A (2020) Hormonal response of Acutodesmus obliquus exposed to combined treatment with 24-epibrassinolide and lead. J Appl Phycol 32:2903–2914
Tarakhovskaya ER, Maslov YI, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physiol 54:163–170
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metals toxicity and the environment. Mol Clin Environ Toxicol 101:133–164
Thomas CE, McLean LR, Parker RA, Ohlweiler DF (1992) Ascorbate and phenolic antioxidant interactions in prevention of liposomal oxidation. Lipids 27:543–550
Tripathi BN, Gaur JP (2004) Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397–404
Tripathi BN, Mehta SK, Amar A, Gaur JP (2006) Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+. Chemosphere 62:538–544
Tripathi RP, Singh B, Bisht SS, Pandey J (2009) L-ascorbic acid in organic synthesis: an overview. Curr Org Chem 13:99–122
Tuteja N, Singh MB, Misra MK, Bhalla PL, Tuteja R (2001) Molecular mechanisms of DNA damage and repair: progress in plants. Crit Rev Biochem Mol Biol 36:337–397
Ugya AY, Imam TS, Li A, Ma J, Hua X (2020) Antioxidant response mechanism of freshwater microalgae species to reactive oxygen species production: a mini review. Chem Ecol 36:174–193
Ulrich K, Jakob U (2019) The role of thiols in antioxidant systems. Free Radic Biol Med 140:14–27
Vara D, Pula G (2014) Reactive oxygen species: physiological roles in the regulation of vascular cells. Curr Mol Med 14:1103–1125
Vishnivetskaya TA (2009) Viable cyanobacteria and green algae from the permafrost darkness. In: Margesin R (ed) Permafrost soils. Springer, Berlin pp 73–84
Volland S, Lütz C, Michalke B, Lütz-Meindl U (2012) Intracellular chromium localization and cell physiological response in the unicellular alga Micrasterias. Aquat Toxicol 109:59–69
Wang W, Yang H, Johnson D, Gensler C, Decker E, Zhang G (2017) Chemistry and biology of ω-3 PUFA peroxidation-derived compounds. Prostagland Other Lipid Mediat 132:84–91
Zbigniew T, Wojciech P (2006) Individual and combined effect of anthracene, cadmium, and chloridazone on growth and activity of SOD izoformes in three Scenedesmus species. Ecotoxicol Environ Saf 65:323–331
Zhang LP, Yang ZM (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419
Zhong Y, Cheng JJ (2017) Effects of selenite on unicellular green microalga Chlorella pyrenoidosa: bioaccumulation of selenium, enhancement of photosynthetic pigments, and amino acid production. J Agric Food Chem 65:10875–10883
Zhu QL, Guo SN, Wen F, Zhang XL, Wang CC, Si LF, Zheng JL, Liu J (2019) Transcriptional and physiological responses of Dunaliella salina to cadmium reveals time-dependent turnover of ribosome, photosystem, and ROS-scavenging pathways. Aquat Toxicol 207:153–162
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Danouche, M., El Ghatchouli, N. & Arroussi, H. Overview of the management of heavy metals toxicity by microalgae. J Appl Phycol 34, 475–488 (2022). https://doi.org/10.1007/s10811-021-02668-w
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DOI: https://doi.org/10.1007/s10811-021-02668-w