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Cadmium effect on physiological responses of the tolerant Chlorophyta specie Picocystis sp. isolated from Tunisian wastewaters

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Abstract

This study aims to investigate the effects of different concentrations of cadmium (Cd) (0–800 μM) on the growth, the photosynthetic performance, and the biochemical parameters of the Chlorophyta Picocystis sp. during 3 and 9 days. Results showed that this exposure did not inhibit the Picocystis growth during the first 3 days of treatment. Growth inhibition did not exceed 53%, which was recorded at high Cd concentrations (800 μM) after nine exposure days. Moreover, no inhibitory effect on the Picocystis sp. photosynthesis has been recorded during the three exposure days regardless the Cd concentrations. Lipid peroxidation was significantly increased at high Cd concentrations (500 and 800 μM) by 40 and 80%, respectively. Furthermore, the highest Cd concentration enhanced the thiol protein content, indicating no consequent protein oxidation. The exposure of Picocystis to Cd stimulated the antioxidant activities of catalase and ascorbate peroxidase. These results showed that Picocystis sp. has an impressive tolerance to Cd stress.

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References

  • Aguilera A, Amils R (2005) Tolerance to cadmium in Chlamydomonas sp. (Chlorophyta) strains isolated from an extreme acidic environment, the Tinto river (SW, Spain). Aquat Toxicol 75:316–329. doi:10.1016/j.aquatox.2005.09.002

    Article  CAS  Google Scholar 

  • Aksmann A, Pokora W, Baścik-Remisiewicz A, Dettlaff-Pokora A, Wielgomas B, Dziadziuszko M, Tukaj Z (2014) Time-dependent changes in antioxidative enzyme expression and photosynthetic activity of Chlamydomonas reinhardtii cells under acute exposure to cadmium and anthracene. Ecotoxicol Environ Safe 110:31–40. doi:10.1016/j.ecoenv.2014.08.005

    Article  CAS  Google Scholar 

  • 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. J Plant Physiol 169:1489–1500. doi:10.1016/j.jplph.2012.06.002

    Article  CAS  Google Scholar 

  • Andosch A, Höftberger M, Lütz C, Lütz-meindl U (2015) Subcellular sequestration and impact of heavy metals on the ultrastructure and physiology of the multicellular freshwater alga Desmidium swartzii. Int J Mol Sci 16:10389–10410. doi:10.3390/ijms160510389

    Article  CAS  Google Scholar 

  • Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  Google Scholar 

  • Ben Chekroun K, Baghour M (2013) The role of algae in phytoremediation of heavy metals: a review. J Mater Environ Sci 4:873–880

    CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • 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). SpringerPlus 2:1–7

    Article  Google Scholar 

  • 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. Ecotoxicol Environ Safe 66:204–209. doi:10.1016/j.ecoenv.2006.02.002

    Article  CAS  Google Scholar 

  • Dalas E, Kallitsis J, Sakkopouos S, Vitoratos E, Koutsoukous PG (1991) Cadmium sulfide precipitation in aqueous media: spontaneous precipitation and controlled overgrowth on polyaniline. J Colloid Interface Sci 141:137–145

    Article  CAS  Google Scholar 

  • Dinakar C, Djilianov D, Bartels D (2012) Photosynthesis in desiccation tolerant plants: energy, metabolism and antioxidative stress defense. Plant Sci 182:29–41. doi:10.1016/j.plantsci.2011.01.018

    Article  CAS  Google Scholar 

  • El-Naggar AH, El-Sheekh MM (1998) Abolishing cadmium toxicity in Chlorella vulgaris by ascorbic acid, calcium, glucose and reduced glutathione. Environ Pollut 101:169–174

    Article  CAS  Google Scholar 

  • Garcia-Rios V, Freile-Pelegrín Y, Robledo D, Mendoza-Cózatl D, Moreno-Sánchez R, Gold-Bouchot G (2007) Cell wall composition affects Cd2 + accumulation and intracellular thiol peptides in marine red algae. Aquat Toxicol 81:65–72. doi:10.1016/j.aquatox.2006.11.001

    Article  CAS  Google Scholar 

  • Huang Z, Li L, Huang G, Yan Q, Shi B, Xu X (2009) Growth-inhibitory and metal-binding proteins in Chlorella vulgaris exposed to cadmium or zinc. Aquat Toxicol 91:54–61. doi:10.1016/j.aquatox.2008.10.003

    Article  CAS  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pfl 167:191–194

    CAS  Google Scholar 

  • Kiran B, Kaushik A, Kaushik CP (2008) Metal-salt co-tolerance and metal removal by indigenous cyanobacterial strains. Proc Biochem 43:598–604. doi:10.1016/j.procbio.2008.01.019

    Article  CAS  Google Scholar 

  • Lamai C, Kruatrachue M, Pokethitiyook P, Upatham ES, Soonthornsarathool V (2005) Toxicity and accumulation of lead and cadmium in the filamentous green alga Cladophora fracta (O.F. Müller Ex Vahl ) Kützing: a laboratory study. Sci Asia 31:121–127

    Article  CAS  Google Scholar 

  • Lewin RA, Krienitz L, Goericke R, Takeda H, Hepperle D (2000) Picocystis salinarum gen. et sp. nov. (Chlorophyta)—a new picoplanktonic green alga. Phycologia 39:560–565

    Article  Google Scholar 

  • Liu W, Ming Y, Li P, Huang Z (2012) Inhibitory effects of hypo-osmotic stress on extracellular carbonic anhydrase and photosynthetic efficiency of green alga Dunaliella salina possibly through reactive oxygen species formation. Plant Physiol Biochem 54:43–48. doi:10.1016/j.plaphy.2012.01.018

    Article  CAS  Google Scholar 

  • Machado MD, Lopes AR, Soares EV (2015) Responses of the alga Pseudokirchneriella subcapitata to long-term exposure to metal stress. J Hazard Mater 296:82–92. doi:10.1016/j.jhazmat.2015.04.022

    Article  CAS  Google Scholar 

  • Mehta SK, Gaur JP (2005) Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit Rev Biotechnol 25:113–152. doi:10.1080/07388550500248571

    Article  CAS  Google Scholar 

  • 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. doi:10.1016/j.plaphy.2006.01.007

    Article  CAS  Google Scholar 

  • Mishra S, Tripathi RD, Srivastava S, Dwivedi S, Trivedi PK, Dhankher OP, Khare A (2009) Thiol metabolism play significant role during cadmium detoxification by Ceratophyllum demersum L. Bioresour Technol 100:2155–2161. doi:10.1016/j.biortech.2008.10.041

    Article  CAS  Google Scholar 

  • Moreno-Garrido I, Lubián LM, Soares AMVM (2000) Influence of cellular density on determination of EC50 in microalgal growth inhibition tests. Ecotoxicol Environ Safe 116:112–116. doi:10.1006/eesa.2000.1953

    Article  Google Scholar 

  • Munter R (2003) Industrial wastewater characteristics. The Baltic University Programme (BUP), Sweden, pp185–194

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299. doi:10.1016/S0168-9452(00)00392-7

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nguyen-Deroche TLN (2008) Effets du cuivre et du zinc sur la photosynthèse et le métabolisme d’une cyanobactérie et de diatomées marines du littoral Vietnamien; comparaison avec des espèces de la côte atlantique française. Univ Maine, Le Mans

    Google Scholar 

  • 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. Bioresour Technol 101:9742–9748. doi:10.1016/j.biortech.2010.07.105

    Article  CAS  Google Scholar 

  • Parker DL, Rai LC, Mallick N, Rai PK, Kumar HD (1998) Effects of cellular metabolism and viability on metal ion accumulation by cultured biomass from a bloom of the cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 64:1545–1547

    CAS  Google Scholar 

  • Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10. doi:10.1016/j.chemosphere.2005.11.024

    Article  CAS  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka E, Godlewska-Żyłkiewicz B (2012) Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol Biochem 52:52–65. doi:10.1016/j.plaphy.2011.11.009

    Article  CAS  Google Scholar 

  • Pokora W, Tukaj Z (2010) The combined effect of anthracene and cadmium on photosynthetic activity of three Desmodesmus (Chlorophyta) species. Ecotoxicol Environ Safe 73:1207–1213. doi:10.1016/j.ecoenv.2010.06.013

    Article  CAS  Google Scholar 

  • Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z (2009a) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquat Toxicol 94:56–61. doi:10.1016/j.aquatox.2009.05.014

    Article  CAS  Google Scholar 

  • Qian H, Xu X, Chen W, Jiang H, Jin Y, Liu W, Fu Z (2009b) Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 75:368–375. doi:10.1016/j.chemosphere.2008.12.040

    Article  CAS  Google Scholar 

  • Ran X, Yue H, Fu X, Kang Y, Xu S, Yang Y, Xu J, Shi J, Wu Z (2015) The response and detoxification strategies of three freshwater phytoplankton species, Aphanizomenon flos-aquae, Pediastrum simplex, and Synedra acus, to cadmium. Enviro Sci Pollut Res 22:19596–19606. doi:10.1007/s11356-015-5161-8

    Article  CAS  Google Scholar 

  • Ravera O (1989) Ecological assessment of environmental degradation, pollution and recovery. Elsevier, Amsterdam

    Google Scholar 

  • Rehman A, Shakoori AR (2004) Tolerance and uptake of cadmium and nickle by Chlorella sp., isolated from tannery effluents. Pakistan J Zool 36:327–331

    CAS  Google Scholar 

  • Rybak A, Messyasz B, Łeska B (2012) Freshwater Ulva (Chlorophyta) as a bioaccumulator of selected heavy metals (Cd, Ni and Pb) and alkaline earth metals (Ca and Mg). Chemosphere 89:1066–1076. doi:10.1016/j.chemosphere.2012.05.071

    Article  CAS  Google Scholar 

  • Sbihi K, Cherifi O, El gharmali A, Oudra B, Aziz F (2012) Accumulation and toxicological effects of cadmium, copper and zinc on the growth and photosynthesis of the freshwater diatom Planothidium lanceolatum (Brébisson) Lange-Bertalot: a laboratory study. J Mater Environ Sci 3:497–506

    CAS  Google Scholar 

  • Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205

    Article  CAS  Google Scholar 

  • Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35:334–346. doi:10.1111/j.1365-3040.2011.02338.x

    Article  CAS  Google Scholar 

  • Shah V (2010) Emerging environmental technologies, volume II. Springer, Dordrecht Heidelberg London doi: 10.1007/978-90-481-3352-9

  • Shi Q, Zhu Z, Xu M, Qian Q, Yu J (2006) Effect of excess manganese on the antioxidant system in Cucumis sativus L. under two light intensities. Environ Exper Bot 58:197–205. doi:10.1016/j.envexpbot.2005.08.005

    Article  CAS  Google Scholar 

  • Silverberg BA (1976) Cadmium-induced ultrastructurel changes in mitochondria of freshwater green algae. Photosynthetica 15:155–159

    CAS  Google Scholar 

  • Singh N, Asthana RK, Kayastha AM, Pandey S, Chaudhary AK, Singh SP (1999) Thiol and exopolysaccharide production in a cyanobacterium under heavy metal stress. Process Biochem 35:63–68. doi:10.1016/S0032-9592(99)00033-3

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaption. Taylor and Francis, London, pp. 445–483

    Google Scholar 

  • Takami R, Almeida JV, Vardaris CV, Colepicolo P, Barros MP (2012) The interplay between thiol-compounds against chromium (VI) in the freshwater green alga Monoraphidium convolutum: toxicology, photosynthesis, and oxidative stress at a glance. Aquat Toxicol 118-119:80–87. doi:10.1016/j.aquatox.2012.03.018

    Article  CAS  Google Scholar 

  • Tukaj Z, Bascik-Remisiewicza A, Skowronski A, Tukaj C (2007) Cadmium effect on the growth, photosynthesis, ultrastructure and phytochelatin content of green microalga Scenedesmus armatus: a study at low and elevated CO2 concentration. Environ Exp Bot 60:291–299. doi:10.1016/j.envexpbot.2006.12.002

    Article  CAS  Google Scholar 

  • Vavilin DV, Ducruet J, Matorin DN, Venediktov PS, Rubin AB (1998) Membrane lipid peroxidation, cell viability and photosystem II activity in the green alga Chlorella pyrenoidosa subjected to various stress conditions. J Photochem Pholobiol B Biol 42:233–239

    Article  CAS  Google Scholar 

  • 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. doi:10.1016/j.aquatox.2011.11.013

    Article  CAS  Google Scholar 

  • Wang S, Zhang D, Pan X (2013) Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. Chemosphere 93:230–237. doi:10.1016/j.chemosphere.2013.04.070

    Article  CAS  Google Scholar 

  • Zarrouk C (1966) Contribution à l’étude d’une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et photosynthèse de Spirulina maxima Geitler. PhD thesis, Univ Paris, France

  • Zhou W, Juneau P, Qiu B (2006) Growth and photosynthetic responses of the bloom-forming cyanobacterium Microcystis aeruginosa to elevated levels of cadmium. Chemosphere 65:1738–1746. doi:10.1016/j.chemosphere.2006.04.078

    Article  CAS  Google Scholar 

  • Zhu X, Zou D, Du H (2011) Physiological responses of Hizikia fusiformis to copper and cadmium exposure. Bot Mar 54:431–439. doi:10.1515/BOT.2011.054

    CAS  Google Scholar 

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Acknowledgments

Authors are thankful to the Team of Microalgal Biotechnology, Nehla Mazhoud, Mohamed Aymen Rajhi, Hannah Ulrich, and Mohamed Aymen Mahjoub for their constructive discussions and valuable help during the preparation of this work.

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Authors and Affiliations

  1. Laboratory of Advanced Materials and Interfaces, Faculty of Medicine, 5019, Monastir, Tunisia

    Ben Ali Rihab & Othmane Ali

  2. National Institute of Marine Sciences and Technology, Team of Microalgal Biotechnology, 5000, Monastir, Tunisia

    Ben Ali Rihab, Ben Ouada Sabrine & Ben Ouada Hatem

  3. Laboratory of Environmental Bioprocesses, Sfax Center of Biotechnology, Sfax, Tunisia

    Ben Ouada Sabrine & Ben Ouada Hatem

  4. UR 09/30: Genetic and Biodiversity, Institute of Biotechnology, 5000, Monastir, Tunisia

    Chouchene Lina & Messaoudi Imed

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  1. Ben Ali Rihab
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  2. Ben Ouada Sabrine
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Correspondence to Ben Ali Rihab.

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Rihab, B.A., Sabrine, B.O., Lina, C. et al. Cadmium effect on physiological responses of the tolerant Chlorophyta specie Picocystis sp. isolated from Tunisian wastewaters. Environ Sci Pollut Res 24, 1803–1810 (2017). https://doi.org/10.1007/s11356-016-7950-0

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