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Heavy Metal Tolerance in Algae

  • Chapter
Algal Adaptation to Environmental Stresses

Abstract

Algae are often exposed to heavy metal pollution due to the disposal of industrial and domestic wastes into waterways. Many algae growing in metal–polluted environments display an ability to tolerate high concentrations of toxic metals (De Filippis and Pallaghy 1994). In fact, even laboratory cultures of some algae can be acclimated to elevated concentrations of toxic metals (Shehata and Whitton 1982; Kuwabara and Leland 1986; Rai et al. 1991; Twiss et al. 1993). Metal tolerance in algae may be genetic or physiological, and the available reports often do not distinguish between these two different sets of mechanisms. The phrases tolerance and resistance have often been used interchangeably, although the latter phrase may be preferred if ability to withstand high concentrations of metals is genetically fixed.

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References

  • Agrawal M, Kumar HD (1975) Response of Chlorella to mercury pollution. Ind J Ecol 21:94–98

    Google Scholar 

  • Ahner BA, Kong S, Morel FMM (1995a) Phytochelatin production in marine algae. 1. An interspecies comparison. Limnol Oceanogr 40: 649–657

    Article  CAS  Google Scholar 

  • Ahner BA, Kong S, Morel FMM (1995b) Phytochelatin production in marine algae. 2. Induction by various metals. Limnol Oceanogr 40: 658–665

    Article  CAS  Google Scholar 

  • Arceneaux JE, Boutwell ME, Byers BR (1984) Enhancement of copper toxicity by siderophores in Bacillus megaterium. Antimicrob Agents Chemother 25: 650–652

    PubMed  CAS  Google Scholar 

  • Asthana RK, Singh AL, Singh SP (1993) Comparison of Ni–sensitive and N–resistant strains of Nostoc muscorum. World J Microbiol Biotechnol 9: 323–327

    Article  CAS  Google Scholar 

  • Bariaud A, Bury M, Mestre JC (1985) Mechanism of Cd2+ resistance in Euglena gracilis. Physiol Plant 63: 382–386

    Article  CAS  Google Scholar 

  • Bernhard W, Kagi JHR (1985) Purification and partial characterisation of atypical cadmium- binding polypeptides from Zea mays. In: Abstr 2nd Int Meet on Metallothionein and Other Low Molecular Weight Metal-Binding Protein. Zurich, Switzerland, 25 pp

    Google Scholar 

  • Chen Z, Ren Q, Shi D, Ru B (1999) Expression of mammalian metallothionein–I gene in cyanobacteria to enhance heavy metal resistance. Mar Pollut Bull 39: 155–158

    Article  CAS  Google Scholar 

  • Clarke SE, Stuart J, Sanders–Loehr J (1987) Induction of siderophore activity in Anabaena spp. and its moderation of copper toxicity. Appi Environ Microbiol 53: 917–922

    CAS  Google Scholar 

  • Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18: 3325–3333

    Article  PubMed  CAS  Google Scholar 

  • Crang RE, Jensen TE (1975) Incorporation of titanium in polyphosphate bodies of Anacystis nidulans. J Cell Biol 67: 80a

    Google Scholar 

  • Crist RH, Oberholser K, Schwartz D, Marzoff J, Ruder D, Crist DR (1988) Interaction of metals and protons with algae. Environ Sci Technol 22: 755–760

    Article  CAS  Google Scholar 

  • Daniel GF, Chamberlain AHL (1981) Copper immobilization in fouling diatoms. Bot Mar 24: 229–243

    Article  CAS  Google Scholar 

  • De Filippis LF (1978) The effect of sublethal concentrations of mercury and zinc on Chlorella. IV. Characteristics of a general reducing enzyme system for metallic ions. Z Pflanzenphysiol 86: 339–352

    Google Scholar 

  • De Filippis LF, Pallaghy CK (1994) Heavy metals: Sources and biological effects. In: Rai LC, Gaur JP, Soeder CJ (eds) Algae and water pollution. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, pp 31–77

    Google Scholar 

  • De Philippis RD, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22: 151–175

    Article  Google Scholar 

  • Eichenberger E (1986) The interaction between essentiality and toxicity of metals in the aquatic ecosystem. In: Metal ions in biological systems, vol 20. Concepts on metal ion toxicity. Marcel Dekker, New York, pp 67–100

    Google Scholar 

  • Erbe JL, Taylor KB, Hall LM (1995) Metalloregulation of the cyanobacterial smt locus: identification of Smt B binding sites and direct interaction with metals. Nucleic Acids Res 23: 2472–2478

    Article  PubMed  CAS  Google Scholar 

  • Erbe JL, Adams AC, Taylor KB, Hall LM (1996a) Cyanobacteria carrying a smt–lux transcriptional fusion as biosensors for the detection of heavy metal cations. J Ind Microbiol 17: 80–83

    Article  PubMed  CAS  Google Scholar 

  • Erbe JL, Taylor KB, Hall LM (1996b) Expression of mouse metallothionein in the cyanobacterium Synechococcus PCC7942. J Ind Microbiol 17: 41–46

    Article  PubMed  CAS  Google Scholar 

  • Ernst WHO, Verkleij JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229– 249

    CAS  Google Scholar 

  • Fiore MF, Trevors JT (1994) Cell composition and metal tolerance in cyanobacteria. BioMetals 7: 83–103

    Article  CAS  Google Scholar 

  • Florence TM, Stauber JL (1986) Toxicity of copper complexes to the marine diatom Nitzschia closterium. Aquat Toxicol 8: 11–26

    Article  CAS  Google Scholar 

  • Fogg GE, Westlake DF (1955) The importance of extracellular products of algae in freshwater. Proc Int Assoc Theor Appi Limnol 12: 2119–2132

    Google Scholar 

  • Foster PL (1977) Copper exclusion as a mechanism of heavy metal tolerance in a green alga. Nature 269: 322–323

    Article  CAS  Google Scholar 

  • Foster PL (1982a) Species associations and metal contents of algae from rivers polluted by heavy metals. Freshwater Biol 12: 17–39

    Article  CAS  Google Scholar 

  • Foster PL (1982b) Metal resistance of Chlorophyta from rivers polluted by heavy metals. Freshwater Biol 12: 41–61

    Article  CAS  Google Scholar 

  • Gekeler W, Grill E, Winnacker E–L, Zenk MH (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Arch Microbiol 150: 197–202

    Article  CAS  Google Scholar 

  • Gekeler W, Grill E, Winnacker E–L, Zenk MH (1989) Survey of the plant kingdom for their ability to bind heavy metals through phytochelatins. Z Naturforsch 44: 361–369

    CAS  Google Scholar 

  • Genter RB (1996) Ecotoxicology of inorganic chemical stress on algae. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology — freshwater benthic ecosystems. Academic Press, California, pp 403–468

    Google Scholar 

  • Genter RB, Cherry DS, Smith EP, Cairns J Jr (1987) Algal-periphyton population and community changes from zinc stress in stream mesocosms. Hydrobiologia 153: 261–275

    Article  CAS  Google Scholar 

  • Gerringa LJA, Rijstenbil JW, Poorvleit TCW, van Drie J, Schot MC (1995) Speciation of copper and responses of the marine diatom Ditylum brightwellii upon increasing copper concentrations. Aquat Toxicol 31: 77–90

    Article  CAS  Google Scholar 

  • Gledhill M, Nimmo M, Hill SJ, Brown MT (1999) The release of copper-compexing ligands by the brown alga Fucus vesiculosus ( Phaeophyceae) in response to increasing total copper levels. J Phycol 35: 501–509

    Google Scholar 

  • Grill E, Winnacker E-L, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230: 674–676

    Article  PubMed  CAS  Google Scholar 

  • Grill E, Gekeler W, Winnacker E-L, Zenk MH (1986) Homophytochelatins are heavy metal- binding peptides of homo-glutathione containing Fabales. FEBS Lett 205: 47–50

    Article  CAS  Google Scholar 

  • Grill E, Winnacker E-L, Zenk MH (1987) Phytochelatins: a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci USA 84: 439–443

    Article  PubMed  CAS  Google Scholar 

  • Grill E, Thumann J, Winnacker E-L, Zenk MH (1988) Induction of heavy-metal-binding phytochelatins by inoculation of cell cultures in standard media. Plant Cell Rep 7: 375–378

    CAS  Google Scholar 

  • Grill E, Löffler S, Winnacker E-L, Zenk MH (1989) Phytochelatins, the heavy-metal binding peptides of plants, are synthesised from glutathione by a specific y-glutamyl- cysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci USA 86: 6838–6842

    Article  PubMed  CAS  Google Scholar 

  • Gupta A, Whitton BA, Morby AP, Huckle JW, Robinson NJ (1992) Amplification and rearrangement of a prokaryotic metallothionein locus smt in Synechococcus PCC 6301 selected for tolerance to cadmium. Proc R Soc Lond B 248: 73–281

    Article  Google Scholar 

  • Gupta A, Morby AP, Turner JS, Whitton BA, Robinson NJ (1993) Deletion within the metallothionein locus of Cd-tolerant Synechococcus PCC 6301 involving a highly iterated palindrome (HIP1). Mol Microbiol 7: 189–195

    Article  PubMed  CAS  Google Scholar 

  • Hall A (1980) Heavy metal cotolerance in a copper tolerant population of the marine fouling alga Ectocarpus siliculosus (Dillw.) Lyngbye. New Phytol 85: 73–78

    Article  CAS  Google Scholar 

  • Hall A, Fielding AH, Butler M (1979) Mechanisms of copper tolerance in the marine fouling alga Ectocarpus siliculosus — evidence for an exclusion mechanism. Mar Biol 54: 195–199

    Article  CAS  Google Scholar 

  • Harding JPC, Whitton BA (1976) Resistance of Stigeoclonium tenue in the field and the laboratory. Br Phycol J 11: 417–426

    Article  Google Scholar 

  • Hashemi F, Leppard GG, Kushner DJ (1994) Copper resistance in Anabaena variabilis: Effects of phosphate nutrition and polyphosphate bodies. Microb Ecol 27: 1159–1176

    Google Scholar 

  • Howe G, Merchant S (1992) Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiol 98: 127–136

    Article  PubMed  CAS  Google Scholar 

  • Huckle JW, Morbey AP, Turner JS, Robinson NJ (1993) Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol Microbiol 7: 177–187

    Article  PubMed  CAS  Google Scholar 

  • Jensen TE, Baxter M, Rachlin JW, Jani V (1982a) Uptake of heavy metals by Plectonema boryanum (Cyanophyceae) into cellular components, especially polyphosphate bodies: an X-ray energy dispersive study. Environ Pollut Ser A Ecol Biol 27: 119–127

    Article  CAS  Google Scholar 

  • Jensen TE, Rachlin JW, Jani V, Warkentine BE (1982b) An X-ray dispersive study of cellular compartmentalization of lead and zinc in Chlorella saccharophila (Chlorophyta), Navícula incerta and Nitzschia closterium ( Bacillariophyta ). Environ Exp Bot 22: 319–328

    Google Scholar 

  • Jin X, Kushner DJ, Nalewajko C (1996) Nickel uptake and release in nickel-resistant and - sensitive strains of Scenedesmus acutus f. alternans ( Chlorophyceae ). Environ Exp Bot 36: 401–411

    Google Scholar 

  • Kagi JHR, Kojima Y (1987) Chemistry and biochemistry of metallothionein. In: Kagi JHR, Kojima Y (eds) Metallothionein II. Birkhäuser, Basel, pp 25–61

    Google Scholar 

  • Kagi JHR, Vallee BL (1960) Metallothionein: a cadmium-and zinc containing protein from equine renal cortex. J Biol Chem 235: 3460–3465

    PubMed  CAS  Google Scholar 

  • Kessler E (1985) An extremely cadmium sensitive strain of Chlorella. Experientia 41: 1621

    Article  CAS  Google Scholar 

  • Knauer K, Behra R, Sigg L (1997) Adsorption and uptake of copper by the green alga Scenedesmus subspicatus ( Chlorophyta ). J Phycol 33: 596–601

    Google Scholar 

  • Kondo N, Isobe M, Imai K, Goto T (1985) Synthesis of metallothionein-like peptides cadystin A and B occurring in fission yeast, and their isomers. Agrie Biol Chem 49: 71–83

    Article  CAS  Google Scholar 

  • Kuwabara JS, Leland HV (1986) Adaptation of Selenastrum capricornutum ( Chloropyceae) to copper. Environ Toxicol Chem 5: 197–203

    Google Scholar 

  • Maclean FI, Lucis OJ, Shaikh ZA, Mansz ER (1972) The uptake and subcellular distribution of Cd and Zn in microorganisms. Fed Proc 31:699

    Google Scholar 

  • Mallick N, Rai LC (1998) Characterisation of Cd-induced low molecular weight protein in a N2-fixing cyanobacterium Anabaena doliolum with special reference to Co-/ multiple tolerance. Biometals 11: 55–61

    Article  CAS  Google Scholar 

  • Mallick N, Rai LC (1999) Respose of the antioxidant system of the nitrogen fixing cyanobacterium Anabaena doliolum to copper. J Plant Physiol 155: 146–149

    CAS  Google Scholar 

  • Mallick N, Pandey S, Rai LC (1994) Involvement of a low molecular weight cadmium binding protein in regulating Cd toxicity in Anabaena doliolum. Biometals 7: 71–83

    Article  Google Scholar 

  • Margoshes M, Vallee BL (1957) A cadmium protein from equine kidney cortex. J Am Chem Soc 79: 4813–4814

    Article  CAS  Google Scholar 

  • McKnight DM, Morel FMM (1979) Release of weak and strong copper–complexing agents by algae. Limnol Oceanogr 24: 823–837

    Article  CAS  Google Scholar 

  • Mehta SK, Gaur JP (1999) Heavy-metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Phytol 143: 253–259

    Article  CAS  Google Scholar 

  • Mehta SK, Tripathi BN, Gaur JP (2000) Influence of pH, culture age and cations on adsorption and uptake of Ni by Chlorella vulgaris. Eur J Protistol 36: 443–450

    Google Scholar 

  • Morby AP, Turner JS, Huckle JW, Robinson NJ (1993) SmfB is a metal regulated repressor of the cyanobacterial metallothionein gene smtk: identification of a Zn inhibited DNA-protein complex. Nucleic Acids Res 21: 921–925

    Article  PubMed  CAS  Google Scholar 

  • Morelli E, Scarano G, Ganni M, Nannicini L, Serriti A (1989) Copper binding ability of the extracellular organic material released by Skeletonema costatum. Chem Spec Bioavail 1:71–76

    CAS  Google Scholar 

  • Murasugi A, Wada C, Hayashi Y (1981) Purification and unique properties in UV and Cd spectra of Cd-binding peptide 1 from Schizosaccharomyces pombe. Biochem Biophys Res Commun 103: 1021–1028

    Article  PubMed  CAS  Google Scholar 

  • Mutoh N, Hayashi Y (1988) Isolation of mutants of Schizosaccharomyces pombe unable to synthesize cadystin, small cadmium-binding peptides. Biochem Biophys Res Commun 151: 32–39

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa M, Takamura Y, Yagi O (1986) Isolation and characterization of the slime from a cyanobacterium Microcystis aeruginosa R-3A. J Agrie Biol Chem 1: 329–337

    Google Scholar 

  • Olafson RW (1984) Prokaryotic metallothionein. Int J Peptide Protein Res 24: 303–308

    Article  CAS  Google Scholar 

  • Olafson RW (1986) Physiological and chemical characterization of cyanobacterial metallothionein. Environ Health Perspect 65: 71–75

    PubMed  CAS  Google Scholar 

  • Olafson RW, Loya S, Sim RG (1980) Physiological parameters of prokaryotic metallothionein induction. Biochem Biophys Res Commun 95: 1495–1503

    Article  PubMed  CAS  Google Scholar 

  • Olafson RW, McCubbin WD, Kay CM (1988) Primary and secondary-structural analysis of a unique prokaryotic metallothionein from a Synechococcus sp. cyanobacterium. Biochem J 251: 691–699

    PubMed  CAS  Google Scholar 

  • Palmiter RD (1987) Molecular biology of metallothionein gene expression. Experientia Suppl 52: 63–80

    PubMed  CAS  Google Scholar 

  • Parker DL, Schram BR, Plude JR, Moore RE (1996) Effect of metal cations on the viscosity of a pectin-like capsular polysaccharide from the cyanobacterium Microcystis flos-aquae C3-40. Appi Environ Microbiol 62: 1208–1213

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Pettersson A, Kunst L, Bergman B, Roomans GM (1985) Accumulation of aluminium by Anabaena cylindrica into polyphosphate granules and cell walls: an X-ray energy-dispersive microanalysis. J Gen Microbiol 131: 2545–2548

    CAS  Google Scholar 

  • Pick U, Ben Amotz A, Karni L, Seebergts CJ, Avron M (1986) Partial characterization of K and Ca uptake systems in the halotolerant alga Dunaliella salina. Plant Physiol 81: 875–881

    Article  PubMed  CAS  Google Scholar 

  • Plude JL, Parker DL, Schommer OJ, Timmerman, RJ, Hagstrom A, Joers JM, Hnasko R (1991) Chemical characterization of polysaccharide from the slime layer of the cyanobacterium Microcystis flos-aquae. Appi Environ Microbiol 57: 1696–1700

    CAS  Google Scholar 

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

    Google Scholar 

  • Rachlin JW, Jensen TE, Warkentine BE (1984) The toxicological response of the alga Anabaena flos-aquae (Cyanophyceae) to cadmium. Arch Environ Contam Toxicol 13:143–151

    Article  CAS  Google Scholar 

  • Rai LC, Gaur JP, Kumar HD (1981a) Phycology and heavy metal pollution. Biol Rev 56:99–151

    Google Scholar 

  • Rai LC, Gaur JP, Kumar HD (1981b) Protective effects of certain environmental factors on the toxicity of zinc, mercury and methylmercury to Chlorella vulgaris Beij. Environ Res 25: 250–259

    Article  PubMed  CAS  Google Scholar 

  • Rai LC, Mallick N, Singh JB, Kumar HD (1991) Physiological and biochemical characteristics of a copper tolerant and a wild-type strain of Anabaena doliolum. J Plant Physiol 138: 68–74

    CAS  Google Scholar 

  • Rauser WE (1990) Phytochelatins. Annu Rev Biochem 59: 61–86

    Article  CAS  Google Scholar 

  • Reed RH, Gadd GM (1990) Metal tolerance in eukaryotic and prokaryotic algae. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 1105–1118

    Google Scholar 

  • Reese RN, Mehra RK, Tarbet EB, Winge DR (1988) Studies on the y-glutamyl Cu-binding peptide from Schizosaccharomyces pombe. J Biol Chem 263: 4186–4192

    PubMed  CAS  Google Scholar 

  • Ren L, Shi D, Dai J, Ru B (1998) Expression of mouse metallthionein-I gene conferring cadmium resistance in a transgenic cyanobacterium.FEMS Microbiol Lett 158: 127–132

    CAS  Google Scholar 

  • Rijstenbil JW, Wijnholds JA (1996) HPLC analysis of non-protein thiols in planktonic diatoms: pool size, redox state and response to copper and cadmium exposure. Mar Biol 127: 45–54

    Article  CAS  Google Scholar 

  • Rijstenbil JW, Derksen JWM, Gerringa LJA, Poortvliet TCW, Sandee A, van den Berg M, van Drie J, Wijnholds JA (1994a) Oxidative stress induced by copper:defense and damage in the marine planktonic diatom Ditylum brightwellii grown in continuous cultures with high and low zinc levels. Mar Biol 119: 583–590

    Article  CAS  Google Scholar 

  • Rijstenbil JW, Sandee A, van Drie J, Wijnholds JA (1994b) Interaction of toxic trace metals and mechanisms of detoxification in the planktonic diatoms Ditylum brightwellii and Thalassiosira pseudonana. FEMS Microbiol Rev 14: 387–396

    Article  PubMed  CAS  Google Scholar 

  • Rijstenbil JW, Dehairs F, Ehrlich R, Wijnholds JA (1998a) Effect of the nitrogen status on copper accumulation and pools of metal-binding peptides in the planktonic diatom Thalassiosira pseudonana. Aquat Toxicol 42: 187–209

    Article  CAS  Google Scholar 

  • Rijstenbil JW, Haritonidis S, Malea P, Seferlis M, Wijnholds JA (1998b) Thiol pools and glutathione redox ratio as possible indicators of copper toxicity in the green macroalgae Enteromorpha spp. from the Scheldt Estuary (SW) Netherlands, Belgium and Thermaikos Gulf ( Greece, N Aegean Sea). Hydrobiologia 385: 171–181

    Google Scholar 

  • Robinson MG, Brown LN (1991) Copper complexation during bloom of Gymnodinium sanguineum Hiraska ( Dinophyceae) measured by ASV. Mar Chem 33: 105–118

    Google Scholar 

  • Robinson NJ (1989) Algal metallothioneins: secondary metabolites and proteins. J Appi Phycol 1: 5–18

    Article  CAS  Google Scholar 

  • Robinson NJ, Jackson PJ (1986) Metallothionein-like metal complexes in angiosperms: their structure and function. Physiol Plant 67: 499–506

    Article  CAS  Google Scholar 

  • Robinson NJ, Ratliff RL, Anderson PJ, Delhaize E, Berger JM, Jackson PJ (1988) Biosynthesis of poly(gamma-glutamylcysteinyl)-glycine in cadmium-resistant Datura innoxia cells. Plant Sci 56: 197–204

    Article  CAS  Google Scholar 

  • Robinson NJ, Gupta A, Fordham-Skelton AP, Croy RRD, Whitton BA, Huckle JW (1990) Prokaryotic metallothionein gene characterisation and expression: chromosome crawling by ligation mediated PCR. Proc R Soc Lond B 242: 241–247

    Article  CAS  Google Scholar 

  • Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. Biochem J 295: 1–10

    PubMed  CAS  Google Scholar 

  • Satoh M, Karaki E, Kakehashi M, Okazaki E, Gotoh T, Oy ama Y (1999) Heavy-metal induced changes in non-proteinaceous thiol levels and heavy-metal-binding peptide in Tetraselmis tetrathele ( Prasinophyceae ). J Phycol 35: 989–994

    Google Scholar 

  • Sauser KR, Liu JK, Wong T-Y (1999) Identification of a copper-sensitive ascorbate peroxidase in the unicellular green alga Selenastrum capricornutum. Biometals 10:163–168 Say PJ, Diaz BM, Whitton BA (1977) Influence of zinc on lotie plants. 1. olerance of Hormidium sp. to zinc. Freshwater Biol 7: 357–376

    Google Scholar 

  • Shaw CF, Petering DH, Weber DN, Gingrich DJ (1989) Inorganic studies of the cadmium- binding peptides from Euglena gracilis. In: Winge D, Hamer D (eds) Metal ion homeostasis. Alan R Liss, New York

    Google Scholar 

  • Shehata FHA, Whitton BA (1982) Zinc tolerance in strains of the blue-green alga Anacystis nidulans. Br Phycol J 17: 5–12

    Article  Google Scholar 

  • Shi J, Lindsay WP, Huckle JW, Morby AP, Robinson NJ (1992) Cyanobacterial metallothionein gene expressed in Escherichia coli-metal-binding properties of the expressed protein. FEBS Lett 303: 159–163

    Article  PubMed  CAS  Google Scholar 

  • Sicko-Goad LM, Stoermer EF (1979) A morphometric study of lead and copper effects on Diatoma tenue var. elongatum ( Bacillariophyta ). J Phycol 15: 316–321

    Google Scholar 

  • Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50: 753–789

    Article  PubMed  CAS  Google Scholar 

  • Silverberg BA, Stokes PM, Ferstenberg LB (1976) Intranuclear complexes in copper tolerant algae. J Cell Biol 69: 210–214

    Article  PubMed  CAS  Google Scholar 

  • Singh S, Pradhan S, Rai LC (1998) Comparative assessment of Fe3+ and Cu2+ biosorption by field and laboratory-grown Microcystis. Process Biochem 33: 495–504

    Article  CAS  Google Scholar 

  • Singh S, Pradhan S, Rai LC (2000) Metal removal from single and multimetallic systems by different biosorbent materials as evaluated by differential pulse anodic stripping voltammetry. Process Biochem 36: 175–182

    Article  CAS  Google Scholar 

  • Singh SP, Yadava V (1986) Cadmium tolerance in the cyanobacterium Anacystis nidulans. Biol Zentralbl 105: 539–542

    CAS  Google Scholar 

  • Skowronski T, De Knecht JA, Simons J, Verkleij JAC (1998) Phytochelatin synthesis in response to cadmium uptake in Vaucheria ( Xanthophyceae ). Eur J Phycol 33: 87–91

    Google Scholar 

  • Starodub ME, Wong PTS, Mayfield CI, Chau YK (1987) Influence of complexation and pH on individual and combined heavy metal toxicities to a freshwater green alga. Can J Fish Aquat Sci 44: 1173–1180

    Article  CAS  Google Scholar 

  • Steffens JC (1990) The heavy metal-binding peptides of plants. Annu Rev Plant Physiol Plant Mol Biol 41: 553–575

    Article  CAS  Google Scholar 

  • Steffens JC, Hunt DF, Williams BG (1986) Accumulation of non-protein metal-binding polypeptides (gamma-glutamyl-cysteinyl)n-glycine in selected cadmium-resistant tomato cells. J Biol Chem 261: 13879–13882

    PubMed  CAS  Google Scholar 

  • Stokes PM (1983) Responses on freshwater algae to metals. In: Round FE, Chapman DJ (eds) Advances in phycological research, vol II. Elsevier, Amsterdam, pp 87–112

    Google Scholar 

  • Stokes PM, Maler T, Riordan JR (1977) A low molecular weight copper-binding protein in a copper tolerant strain of Scenedesmus acutiformis. In: Hemphil DD (ed) Trace substances in environmental health. University of Missouri Press, Columbia, pp 146–154

    Google Scholar 

  • Takamura N, Kasai F, Watanabe MM (1989) Effects of Cu, Cd and Zn on photosysnthesis of freshwater benthic algae. J Appi Phycol 1: 39–52

    Google Scholar 

  • Tease BC, Walker R (1987) Comparative composition of the sheath of the cyanobacterium Gloeothece ATCC 27512 cultured with and without combined nitrogen. J Gen Microbiol 133: 3331–3339

    CAS  Google Scholar 

  • Tillberg JE, Barnard T, Rowley JR (1984) Phosphorus status and cytoplasmic structure in Scenedesmus ( Chlorophyceae) under different metabolic regimes. J Phycol 20: 124–136

    Google Scholar 

  • Ting YP, Teo WK, Soh CY (1995) Gold uptake by Chlorella vulgaris. J Appi Phycol 7: 97–100

    Article  CAS  Google Scholar 

  • Turner JS, Robinson NJ (1995) Cyanobacterial metallothioneins: biochemistry and molecular genetics. J Ind Microbiol 14:119002D125

    Google Scholar 

  • Turner JS, Morby AP, Whitton BA, Gupta A, Robinson NJ (1993) Construction and characterisation of Zn2+/Cd2+ hypersensitive cyanobacterial mutants lacking a functional metallothionein locus. J Biol Chem 268: 4494–4498

    PubMed  CAS  Google Scholar 

  • Twiss MR, Nalewajko C (1992) Influence of phosphorus nutrition on copper toxicity to three strains of Scenedesmus acutus ( Chlorophyceae ). J Phycol 28: 291–298

    Google Scholar 

  • Twiss MR, Welbourn PM, Schwärtzel E (1993) Laboratory selection of copper tolerance in Scenedesmus acutus ( Chlorophyceae ). Can J Bot 71: 333–338

    Google Scholar 

  • Vangronsveld J, Clijsters H (1994) Toxic effects of metals. In: Farago ME (ed) Plants and the chemical elements: biochemistry, uptake, tolerance and toxicity. VCH Verlagsgesellschaft, Weinheim, pp 149–177

    Google Scholar 

  • Verma SK, Singh HN (1991) Evidence for energy–dependent copper efflux as a mechanism of Cu2+ resistance in the cyanobacterium Nostoc caldcóla. FEMS Microbiol Lett 84: 291–294

    Article  CAS  Google Scholar 

  • Vogeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Plant Physiol 92:1086–1093

    Google Scholar 

  • Wagatsuma T, Akiba R (1989) Low surface negativity of root protoplasts from aluminum- tolerant species. Soil Sci Plant Nutrition 35: 443–452

    CAS  Google Scholar 

  • Weber DN, Shaw CF, Petering DH (1987) Euglena gracilis cadmium-binding protein-II contains sulfide ion. J Biol Chem 262:6962–6964

    PubMed  CAS  Google Scholar 

  • Weckesser J, Hoffmann K, Jürgens UJ, Whitton BA (1988) Isolation and chemical analysis of the sheaths of the filamentous cyanobacteria Calothrix parietina and C. scopulorum. J Gen Microbiol 134: 629–634

    CAS  Google Scholar 

  • Whitton BA (1970) Toxicity of heavy metals to Chlorophyta from running waters. Arch Mikrobiol 72: 353–360

    PubMed  CAS  Google Scholar 

  • Whitton BA (1980) Zinc and plants in rivers and streams. In: Nriagu JO (ed) Zinc in the environment, Part II Health effects. John Wiley, New York, pp 364–400

    Google Scholar 

  • Whitton BA, Say PJ (1975) Heavy metals. In: Whitton BA (ed) River ecology. Blackwell, Oxford, pp 286–311

    Google Scholar 

  • Winter C, Winter M, Pohl P (1994) Cadmium adsorption by non-living biomass of the semi- macroscopic alga, Ectocarpus siliculosus, grown in axenic mass culture and localisation of the adsorbed Cd by transmission electron microscopy. J Appi Phycol 6: 479–487

    Article  CAS  Google Scholar 

  • Wong SL, Nakamoto L, Wainwright JF (1994) Identification of toxic metals in affected algal cells in assay of wastewaters. J Appi Phycol 6: 405–414

    Article  CAS  Google Scholar 

  • Woolhouse HW (1983) Toxicity and tolerance in the response of plants to metals. In: Lange O, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology. Ill Responses to the chemical and biological environment. Springer, Berlin Heidelberg New York, pp 125–300

    Google Scholar 

  • Wu J-T, Chang S-C, Chen K-S (1995) Enhancement of intracellular proline level in cells of Anacystis nidulans ( Cyanobacteria) exposed to deleterious concentrations of copper. J Phycol 31: 376–379

    Article  CAS  Google Scholar 

  • Wu J-T., Hsieh M-T, Kow L-C (1998) Role of proline accumulation in response to toxic copper in Chlorella sp. ( Chlorophyceae ). J Phycol 34: 113–117

    Article  Google Scholar 

  • Xue H-B, Sigg L (1990) Binding of Cu ( II) to algae in a metal buffer. Water Res 24: 1129–1136

    Article  CAS  Google Scholar 

  • Yoshimura E, Nagasaka S, Sato Y, Satake K, Mori S (1999) Extraordinary high aluminium tolerance of the acidophilic alga, Cyanidium caldarium. Soil Sci Plant Nutr 45: 721–724

    CAS  Google Scholar 

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  1. Department of Botany, Banaras Hindu University, Varanasi, 221 005, India

    L. C. Rai

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  1. J. P. Gaur
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  1. Department of Botany, Banaras Hindu University, 221 005, Varanasi, India

    Lal Chand Rai  & Jai Prakash Gaur  & 

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Gaur, J.P., Rai, L.C. (2001). Heavy Metal Tolerance in Algae. In: Rai, L.C., Gaur, J.P. (eds) Algal Adaptation to Environmental Stresses. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59491-5_12

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  • DOI: https://doi.org/10.1007/978-3-642-59491-5_12

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