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The sensitivity of two Monoraphidium species to zinc: their possible future role in bioremediation

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Abstract

Effects of zinc on growth, cell morphology, oxidative stress responses and zinc removal activity of two common phytoplankton species, Monoraphidium pusillum (Printz) Komárková-Legnerová and Monoraphidium griffithii (Berkeley) Komárková-Legnerová were investigated at a concentration range of 0.2–160 mg l−1 zinc. Cell densities and chlorophyll content decreased compared with controls in cultures of both species, effective concentrations causing 50 % growth inhibition within 72 h on the basis of cell numbers were 33.69 and 25.63 mg l−1 zinc for M. pusillum and M. griffithii, respectively. Changes in cell morphology and elevated lipid peroxidation levels appeared in zinc-treated cultures of both species, but only at higher (>10 mg l−1) zinc concentrations. The most effective zinc removal appeared at 20 and 10 mg l−1 zinc concentration for M. pusillum and M. griffithii, respectively. Removed zinc is mainly bound on the cell surface in the case of both species. This study provides new data for the zinc tolerance and zinc removal ability of the green algae M. pusillum and M. griffithii and shows that green algal species common in surface waters could have zinc tolerance and zinc-binding abilities, which makes them feasible in treatment of waters contaminated with 10–20 mg l−1 zinc.

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References

  • Ahuja P, Gupta R, Saxena RK (1999) Zn2+ biosorption by Oscillatoria angustissima. Proc Biochem 34:77–85

    Article  CAS  Google Scholar 

  • Ahuja P, Mohapatra H, Saxena RK, Gupta R (2001) Reduced uptake as a mechanism of zinc tolerance in Oscillatoria angustissima. Curr Microbiol 43:305–310

    Article  CAS  Google Scholar 

  • Andrade LR, Farina M, Amado-Filho GM (2004) Effects of copper on Enteromorpha flexuosa (Chlorophyta) in vitro. Ecotoxicol Environ Saf 58:117–125

    Article  CAS  Google Scholar 

  • Bates SS, Tessier A, Campbell PGC, Buffle J (1982) Zinc adsorption and transport by Chlamydomonas variabilis and Scenedesmus subspicatus (Chlorophyceae) grown in semicontinuous culture. J Phycol 18:521–529

    Article  CAS  Google Scholar 

  • Bird G, Brewer PA, Macklin MG, Balteanu D, Driga B, Serban M, Zaharia S (2003) The solid state partitioning of contaminant metals and As in river channel sediments of the mining affected Tisa drainage basin, northwestern Romania and eastern Hungary. Appl Geochem 18:1583–1595

    Article  CAS  Google Scholar 

  • Brinza L, Dring MJ, Gavrilescu M (2007) Marine micro- and macro-algal species as biosorbents for heavy metals. Environ Eng Manag J 6:237–251

    CAS  Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  Google Scholar 

  • Chojnacka K (2010) Biosorption and bioaccumulation—the prospects for practical applications. Environ Int 36:299–307

    Article  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatin and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  • Cotton FA, Wilkinson G, Murillo CA, Bochmann M (1999) Advanced inorganic chemistry, 6th edn. John Wiley & Sons Inc., New York

    Google Scholar 

  • Das N (2010) Recovery of precious metals through biosorption—a review. Hydrometallurgy 103:180–189

    Article  CAS  Google Scholar 

  • de Bashan LE, Bashan Y (2010) Immobilized microalgae for removing pollutants: review of practical aspects. Bioresource Technol 101:1611–1627

    Article  Google Scholar 

  • de Queiroz JC, de Melo Ferreira AC, da Costa ACA (2012) The growth of Monoraphidium sp. and Scenedesmus sp. cells in the presence of thorium. Sci World J. doi:10.1100/2012/592721

    Google Scholar 

  • Eisler R (1993) Zinc hazard to fish, wildlife, and invertebrates: a synoptic review. Contam Hazard Rev 10:1–126

    Google Scholar 

  • Felföldy L (1987) A biológiai vízminősítés. 4. kiad. In: Vízügyi Hidrobiológia 16. VGI, Budapest, 258

  • Fosmire GJ (1990) Zinc toxicity. Am J Clin Nutr 51:225

    CAS  Google Scholar 

  • Fujii K, Nakashima H, Hashidzume Y, Uchiyama T, Mishiro K, Kadota Y (2009) Nutritional profile of Monoraphidium sp. GK12, astaxanthin-producing microalga, and its energy-saving outdoor cultivation. J Biosci Bioeng 108(1):S44

    Article  Google Scholar 

  • Fukami M (1988) Effects of zinc on metal metabolism on the zinc tolerant chlorotic mutants of Euglena gracilis. J Agric Biol Chem 52:2343–2344

    Article  CAS  Google Scholar 

  • Gattullo CE, Bährs H, Steinberg CEW, Loffredo E (2012) Removal of bisphenol A by the freshwater green alga Monoraphidium braunii and the role of natural organic matter. Sci Total Environ 416:501–506

    Article  CAS  Google Scholar 

  • Gold C, Feurtet-Mazel A, Coste M, Boudou A (2003) Impacts of Cd and Zn on the development of periphytic diatom communities in artificial streams located along a river pollution gradient. Arch Environ Contam Toxicol 44:189–197

    Article  CAS  Google Scholar 

  • Hammer Ř, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Hassler CS, Behra R, Wilkinson KJ (2005) Impact of zinc acclimation on bioaccumulation and homeostasis in Chlorella kesslerii. Aquat Toxicol 74:139–149

    Article  CAS  Google Scholar 

  • Hornstrom E, Harbom A, Edberg F, Andren C (1995) The influence of pH on aluminium toxicity in the phytoplankton species Monoraphidium dybowskii and M. griffithii. Water Air Soil Poll 85(2):817–822

    Article  Google Scholar 

  • Horváth B, Gruiz K (1996) Impact of metalliferous ore mining activity on the environment in Gyongyosoroszi, Hungary. Sci Total Environ 184:215–227

    Article  Google Scholar 

  • Hussein H, Farag SI, Kamal K, Moawad H (2004) Biosorption of heavy metals from waste water using Pseudomonas sp. Electron J Biotechnol 7(1):39–46

    Article  Google Scholar 

  • Kapoor A, Viraraghavan T (1995) Fungal biosorption—an alternative treatment option for heavy metal bearing wastewater: a review. Bioresour Technol 53(3):195–206

    CAS  Google Scholar 

  • Lehmann V, Tubbing GMJ, Admiraal W (1998) Induced metal tolerance in microbenthic communities from three lowland rivers with different metal loads. Arch Environ Contam Toxicol 36:384–391

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Malea P, Rijstenbil JW, Haritonidis S (2006) Effects of cadmium, zinc and nitrogen status on non-protein thiols in the macroalgae Enteromorpha spp. from the Scheldt Estuary (SW Netherlands, Belgium) and Thermaikos Gulf (N Aegean Sea, Greece). Mar Environ Res 62:45–60

    Article  CAS  Google Scholar 

  • Monteiro CM, Marques APGC, Castro PML, Malcata FX (2009) Characterization of Desmodesmus pleiomorphus isolated from a heavy metal-contaminated site: biosorption of zinc. Biodegradation 20:629–641

    Article  CAS  Google Scholar 

  • Monteiro CM, Fonseca SC, Castro PML, Malcata FX (2011a) Toxicity of cadmium and zinc on two microalgae, Scenedesmus obliquus and Desmodesmus pleiomorphus, from Northern Portugal. J Appl Phycol 23:97–103

    Article  CAS  Google Scholar 

  • Monteiro CM, Castro PML, Malcata FX (2011b) Biosorption of zinc ions from aqueous solution by the microalga Scenedesmus obliquus. Environ Chem Lett 9:169–176

    Article  CAS  Google Scholar 

  • Morin S, Coste M (2006) Metal-induced shifts in the morfology of diatoms from Riou Mort and Riou Vioi streams (South West France). Arch Hydrobiol—Supplement 97–101

  • Munoz R, Guieysse B (2006) Algal-bacterial processes for the treatment of hazardous contaminants: a review. Water Res 40:2799–2815

    Article  CAS  Google Scholar 

  • Muyssen BTA, De Schamphelaere KAC, Janssen CR (2006) Mechanisms of chronic waterborne Zn toxicity in Daphnia magna. Aquat Toxicol 77:393–401

    Article  CAS  Google Scholar 

  • Nacorda JO, Martinez-Goss MR, Torreta NK, Merca FE (2007) Metal resistance and removal by two strains of the green alga, Chlorella vulgaris Beijerinck, isolated from Laguna de Bay, Philippines. J Appl Phycol 19:701–710

    Article  CAS  Google Scholar 

  • Nishikawa K, Tominaga N (2001) Isolation, growth, ultrastructure, and metal tolerance of the green alga Chlamydomonas acidophila (Chlorophyta). Biosci Biotechnol Biochem 65:2650–2656

    Article  CAS  Google Scholar 

  • Ódor L, Richard BW, Horváth I, Fügedi U (1998) Mobilization and attenuation of metals downstream from a base-metal mining site in the Mátra Mountains, northeastern Hungary. J Geochem Explor 65:47–60

    Article  Google Scholar 

  • Omar HH (2002) Bioremoval of zinc ions by Scenedesmus obliquus and Scenedesmus quadricauda and its effect on growth and metabolism. Int biodeterior Biodegrad 50:95–100

    Article  CAS  Google Scholar 

  • Palmieria MC, Garcia O, Melnikov P (2000) Neodymium biosorption from acidic solutions in batch system. Process Biochem 36:441–444

    Article  Google Scholar 

  • Pawlik-Skowrońska B (2003) Resistance, accumulation and allocation of zinc in two ecotypes of the green alga Stigeoclonium tenue Kütz. coming from habitats of different heavy metal concentrations. Aquat Bot 75:189–198

    Article  Google Scholar 

  • Perales-Vela HV, Pena-Castro JM, Canizares-Villaneuva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10

    Article  CAS  Google Scholar 

  • Perovic S, Tretter L, Brummer F, Wetzler C, Brenner J, Donner G, Schroder HC, Muller WEG (2000) Dinoflagellates from marine algal blooms produce neurotoxic compounds: effects on free calcium levels in neuronal cells and synaptosomes. Environ Toxicol Pharmacol 8(2):83–94

    Article  CAS  Google Scholar 

  • Pradhan S, Sing S, Rai LC, Parker DL (1998) Evaluation of metal biosorption efficiency of laboratory-grown Microcystis under various environmental conditions. J Microbiol Biotechnol 8:53–60

    Google Scholar 

  • Prasad AS (2008) Zinc in human health: effect of zinc on immune cells. Mol Med 14:353

    Article  CAS  Google Scholar 

  • Romera E, Gonzalez F, Ballester A, Blazquez ML, Munoz JA (2006) Biosorption with algae: a statistical review. Crit Rev Biotechnol 26:223–235

    Article  CAS  Google Scholar 

  • Romera E, González F, Ballester A, Blázquez ML, Muñoz JA (2007) Comparative study of biosorption of heavy metals using different types of algae. Bioresour Technol 98:3344–3353

    Article  CAS  Google Scholar 

  • Schmitt D, Müller A, Csögör Z, Frimmel FH, Posten C (2001) The adsorption kinetics of metal ions onto different microalgae and siliceous earth. Water Res 35:779–785

    Article  CAS  Google Scholar 

  • Sugarman B (1983) Zinc and infection. Rev Infect Dis 5:137

    Article  CAS  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

    Article  Google Scholar 

  • Travieso L, Canizares RO, Borja R, Benitez F, Dominguez AR, Dupeyron R, Valiente V (1999) Heavy metal removal by microalgae. Bull Environ Contam Toxicol 62:144–151

    Article  CAS  Google Scholar 

  • Tripathi BN, Gaur JP (2004) Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397–404

    Article  CAS  Google Scholar 

  • Tripathi BN, Gaur JP (2006) Physiological behavior of Scenedesmus sp. during exposure to elevated levels of Cu and Zn and after withdrawal of metal stress. Protoplasma 229:1–9

    Article  CAS  Google Scholar 

  • Tsuji N, Hirayanagi N, Okada M, Miyasaka H, Hirata K, Zenk MH, Miyamotoa K (2002) Enhancement of tolerance to heavy metals and oxidative stress in Dunaliella tertiolecta by Zn-induced phytochelatin synthesis. Biochem Biophys Res Commun 293:653–659

    Article  CAS  Google Scholar 

  • Vasas G, Bácsi I, Surányi G, Hamvas MM, Mathe C, Nagy SA, Borbely G (2010) Isolation of viable cell mass from frozen Microcystis viridis bloom containing microcystin-RR. Hydrobiologia 639:147–151

    Article  CAS  Google Scholar 

  • Vasas G, M-Hamvas M, Borics G, Gonda S, Mathe C, Jambrik K, Nagy ZL (2012) Occurrence of toxic Prymnesium parvum blooms with high protease activity is related to fish mortality in Hungarian ponds. Harmful Algae 17:102–110

    Article  Google Scholar 

  • Vasas G, Farkas O, Borics G, Felföldi T, Sramkó G, Batta G, Bácsi I, Gonda S (2013) Appearance of Planktothrix rubescens Bloom with [D-Asp3, Mdha7]MC–RR in Gravel Pit Pond of a Shallow Lake-dominated area. Toxins 5:2434–2455

    Article  CAS  Google Scholar 

  • Vavilin DV, Ducruet JM, 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 Photobiol B Biol 42:233–239

    Article  CAS  Google Scholar 

  • Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164(4):645–655

    Article  CAS  Google Scholar 

  • Visviki I, Rachlin JW (1991) The toxic action and interactions of copper and cadmium to the marine alga Dunaliella minuta, in both acute and chronic exposure. Arch Environ Contam Toxicol 20:271–275

    Article  CAS  Google Scholar 

  • Volesky B (1990a) Biosorption and biosorbents. In: Biosorption of heavy metals. CRC press, Boston

  • Volesky B (1990b) Removal and recovery of heavy metals by biosorption. In: Biosorption of heavy metals. CRC press, Boston

  • Wang JL, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotech Adv 27:195–226

    Article  Google Scholar 

  • Yang X, Liu P, Hao Z, Shi J, Zhang S (2012) Characterization and identification of freshwater microalgal strains toward biofuel production. Bioresources 7(1):686–695

    CAS  Google Scholar 

  • Yu X, Zhao P, He C, Li J, Tang X, Zhou J, Huang Z (2012) Isolation of a novel strain of Monoraphidium sp. and characterization of its potential application as biodiesel feedstock. Bioresour Technol 121:256–262

    Article  CAS  Google Scholar 

  • Zar JH (1996) Biostatical analysis, 3rd edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Zhang QC, Qiu LM, Yu RC, Kong FZ, Wang YF, Yan T, Gobler CJ, Zhou MJ (2012) Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae 19:117–124

    Article  Google Scholar 

Download references

Acknowledgments

The research was supported by the EU and co-financed by the European Social Fund under the project ENVIKUT (TÁMOP-4.2.2.A-11/1/KONV-2012-0043), by the Internal Research Project of the University of Debrecen and by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences.

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Authors and Affiliations

  1. Department of Hydrobiology, University of Debrecen, Egyetem tér 1, 4032, Debrecen, Hungary

    I. Bácsi, Z. Novák, I. Grigorszky & S. A. Nagy

  2. Environmental Protection and Nature Conservation Authority, Trans-Tiszanian Region, Hatvan u. 16, 4025, Debrecen, Hungary

    M. Jánószky & V. B-Béres

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  1. I. Bácsi
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  2. Z. Novák
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Correspondence to I. Bácsi.

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Bácsi, I., Novák, Z., Jánószky, M. et al. The sensitivity of two Monoraphidium species to zinc: their possible future role in bioremediation. Int. J. Environ. Sci. Technol. 12, 2455–2466 (2015). https://doi.org/10.1007/s13762-014-0647-3

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  • DOI: https://doi.org/10.1007/s13762-014-0647-3

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