TOLERANCE AGAINST HEAVY METAL TOXICITY IN CYANOBACTERIA: ROLE OF ANTIOXIDANT DEFENSE SYSTEM
The toxicity of heavy metals is reviewed with reference to Cyanobacteria. Cyanobacteria also known as blue green algae are primitive photosynthetic prokaryotic microorganism which has high economic importance due to various bioactive compounds. Cyanobacteria are exposed to heavy metal stress since these are widely distributed. Heavy metal enters into the cell through various interactions between metal ions and functional groups present at the cell surface and cause toxicity. Heavy metals also cause oxidative stress by generation of reactive oxygen species, including superoxide, hydrogen peroxide and hydroxyl radical which are highly reactive and toxic and cause damage to nucleic acid, protein, and lipid. Cyanobacteria have evolved strategies to overcome the effect of reactive oxygen species that include antioxidant enzymes such as superoxide dismutase, catalase, ascorbate peroxidase and Glutathione reductase.
2. Ghosh M, Singh SP. Review on phytoremediation of heavy metals and utilization of its by products. Appl Ecol Res 2005;3:1-18.
3. Jadhav JP, Kalyani DC, Telke AA, Phugare SS, Govindwar SP. Evaluation of the efficacy of a bacterial consortium for the removal of color, reduction of heavy metals, and toxicity from textile dye effluent. Bioresour Technol 2010;101:165-73.
4. Ann C, Karen S, Jos R, Kelly O, Els K, Tony R, et al. The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 2011;168:309â€“16.
5. Aravind P, Prasad MNV, Malec P, Waloszek A, Strzalka K. Zinc protects Ceratophyllum demersum L. (free floating hydrophyte) against reactive oxygen species induced by cadmium. J Trace Elem Med Biol 2009;23:50â€“60.
6. Gangwar S, Singh VP, Srivastava PK, Maurya JN. Modification of chromium (VI) phytotoxicity by exogenous gibberellic acid application in Pisum sativum (L.) seedlings. Acta Physiol Plant 2011;33:1385â€“97.
7. Huang H, Gupta DK, Tian S, Yang X, Li T. Lead tolerance and physiological adaptation mechanism in roots of accumulating and non-accumulating ecotypes of Sedum alfredii. Environ Sci Pollut Res 2012;19:1640â€“51.
8. Kanoun-Boule M, Vicente JAF, Nabais C, Prasad MNV, Freitas H. Ecophysiological tolerance of duckweeds exposed to copper. Aquat Toxicol 2009;91:1â€“9.
9. Kulasooriya SA. Cyanobacteria: pioneers of planet earth. Ceylon J Sci (Biol Sci) 2011;40:71-88.
10. Dias MA. Removal of heavy metals by an Aspergillus terreus strain immobilized in polyurethane matrix. Lett Appl Microbiol 2002;34:46-50.
11. Lenntech Water Treatment and Air Purification: Water Treatment Published by Lenntech, Rotterdamseweg, Netherlands; 2004.
12. Weast RC. CRC handbook of chemistry and physics, 64th edn. CRC Press, Boca Raton; 1984.
13. Athar M, Vohora SB. Heavy metals and environment, New Delhi, New Age International Publisher; 2001. p. 3-40.
14. Inthorn D. Removal of heavy metal by using microalgae. Edited by hiroyuki kojima and yuan kun lee, photosynthetic microorganisms in environmental biotechnology. Springer Verlag Hong Kong Ltd 2001;310:111-69.
15. Ash C, Stone R. A question of dose. Sci 2003;300(5621):849-1036.
16. Allan R. Mining and metals in the environment. J Geochem Explor 1997;58(2):95â€“100.
17. Holum JR. Elements of General and Biological Chemistry, 6th Edition, John Wiley and Sons NY; 1983. p. 324, 326, 353, 469.
18. McCluggage D. Heavy Metal Poisoning, NCS Magazine, Published by The Bird Hospital, CO, USA; 1991.
19. Dayan AD, Paine AJ. Mechanisms of chromium toxicity, carcinogenicity and allergenicity. Hum Expos Toxicol 2001;20:439â€“51.
20. Patrick L. Lead toxicity, a review of the literature. Part 1: Exposure, evaluation, and treatment. Altern Med Rev 2006;11:2â€“22.
21. Trueby P. Impact of Heavy Metals on Forest Trees From Mining Areas. In: International Conference on Mining and The Environment III, Sudbury, Ontario, Canada; 2003.
22. Mudgal V, Madaan N, Mudgal A, Singh RB, Mishra S. Effect of toxicmetals on human health. Open Nutr 2010;3:94â€“9.
23. Saha N, Zaman MR. Evaluation of possible health risks of heavy metals by consumption of foodstuffs available in the central market of Rajshahi City, Bangladesh. Environ Monit Assess 2012;185:3867-78.
24. Hadson PV. The effect of metabolism on uptake, disposition and toxicity in fish. Aquat Toxicol 1988;11:3â€“18.
25. Akoto O, Bismark Eshun F, Darko G, Adei E. Concentrations and health risk assessments of heavy metals in fish from the fosu lagoon. Int J Environ Res 2014;8(2):403-10.
26. Terra BF, AraÃºjo FG, Calza CF, Lopes RT, Teixeira TP. Heavy metal in tissues of three fish species from different trophic levels in a tropical brazilian river. Water Air Soil Pollut 2007;187:275-84.
27. Yilmaz AB. Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugil cephalus and Trachurus mediterraneus from Iskenderun Bay, Turkey. Environ Res 2003;92:277â€“81.
28. Al-Busaidi M, Yesudhanon P, Al-Mughairi S, Al-Rahbi WAK, Al-harthy KS, Al-Mazrooei NA, et al. Toxic metals in commercial marine fish in Oman with reference of national and international standards. Chemosphere 2011;85:67â€“73.
29. Emami Khansari F, Ghazi-Khansari M, Abdollahi M. Heavy metals content of canned tuna fish. Food Chem 2005;93:293-6.
30. Landis GW, Ming-Ho Yu. Introduction to Environmental Toxicology: Impacts of Chemicals Upon Ecological Systems. CRC Press, Lewis Publishers, Boca Raton, Fl; 2003.
31. Palmer CD, Puls RW. Natural attenuation of hexavalent chromium in ground water and Soils. USEPA Ground Water Issue, EPA/540/5-94/505, U. S. Govt. Print. Office, Washington, DC; 1994. p. 57-72.
32. Vincent WF. Cyanobacteria. Laval University, Quebec City, QC, Canada Elsevier Inc; 2009. p. 226-32.
33. Azolla Utilization: Proceedings of the Workshop on Azolla Use, Fuzhou, Fujian, China 1985. The International Rice Research Institute, Los Banos, Philippines; 1987. p. 296.
34. Venkataraman GS. Algal Biofertilizers and Rice Cultivation. Today and Tomorrows Printers and Publishers, Calcutta; 1972. p. 81.
35. Habib MAB, Parvin M, Huntington TC, Hasan MR. A review on culture, production and use of spirulina as food for humans and feeds for domestic animals and fish. FAO Fisheries and Aquaculture Circular. No. 1034. Rome, FAO; 2008. p. 33.
36. Namiki M. Antioxidant/ antimutagenics in food. In: CRC. Crit Rev Food Sci Nutr 1990;29:273-300.
37. Mirada MS, Cintra RG, Barros SM, Mancini-Filho J. Antioxidant activity of microalga Spirulina maxima. Braz J Med Biol Res 1998;31:1075-9.
38. Pratt DE. Natural antioxidants from plant material, Phenolic compounds: Food and their effects on health. Am Chem Soc, Washington, (ACS Symposium Series 1992;507:54-71.
39. Robbins J. Anti-inflammatory and Antioxidant effects. Diet for A new America; 1987. p. 20.
40. Sudha SS, Karthic R, Francis M, Soumya TS, Ramanujam JR. Associated microoorganisms from spirulina p-roducts. Isolation and preliminary characterization of associated microorganisms from Spirulina products and their silver mediated nanoparticle synthesis. J Algal Biomass Utln 2011;2:1â€“8.
41. Perales-Vela HV, PenËœa-Castro J, CanËœizares-Villanueva RO. Heavy metal detoxification in eukaryotic microalgae. Chemosphere 2006;64:1-10.
42. Cobbett C, Goldsbrough P. Phytochelatin and metallothioneins: Roles in heavy metal detoxification and homeostasis. Ann Rev Plant Biol 2002;53:159â€“82.
43. Liu RX, Tang HX, Lao WX. Advances in bio-sorption mechanism and equilibrium modeling for heavy metals on biomaterials. Prog Chem 2002;14:87-92.
44. Goyal N, Jain SC, Banerjee UC. Comparative studies on the microbial adsorption of heavy metals. Adv Environ Res 2003;7:311-9.
45. Arunakumara KKIU, Xuecheng Z. Heavy metal bioaccumulation and toxicity with special reference to microalgae. J Ocean Univ Chin 2008;7:25-30.
46. Wang J, Chen C. Biosorption of heavy metals by Saccharomyces cerevisiae. Biotech Adv 2006;24:427-51.
47. Babu RL, Vijayalakshmi E, M Naveen Kumar, Patil RH, Devaraju KS, Sharma SC. Biosorption of Chromium(VI) and Lead(II): Role of Spirulina platensis in the Treatment of Industrial Effluent. Biorem J 2013;17(4):231-9.
48. Balaji S, Kalaivani T, Rajasekaran C, Shalini M, Siva R, Singh RK, et al. Arthrospira (Spirulina) species as bioadsorbents for lead, chromium and cadmiumâ€“a comparative study. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim; 2014.
49. Pandi M, Shashirekha V, Swamy M. Bioabsorption of chromium from retan chrome liquor by cyanobacteria. Microbiol Res 2009;164:420-8.
50. Tripathi BN, Gaur JP. Physiological behavior of Scenedesmus sp. during exposure to elevated levels of Cu and Zn and after withdrawal of metal stress. Protoplasma 2006;229:1-9.
51. Choudhury S, Panda SK. Toxic effects, oxidative stress and ultrastructural changes in moss Taxithelium nepalense (Schwaegr.) Broth under chromium and lead phytotoxicity. Water Air Soil Pollut 2005;167:73-90.
52. Choudhary M, Jetley UK, Khana MA, Zutshi N, Fatma T. Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotoxicol Environ Saf 2007;66(2):204-9.
53. Jiunn-Tzong W, Chang S, Chou T. Intracellular proline accumulation in some algae exposed to Copper and Cadmium. Bot Bull Acad Sin 1995;36:89-93.
54. Rai UN, Singh NK, Upadhyay AK, Verma S. Chromate tolerance and accumulation in Chlorella vulgaris L: role of antioxidant enzymes and biochemical changes in detoxification of metals. Bioresour Technol 2013;136:604â€“9.
55. Deniz F, Saygider SD, Karaman S. Response to copper and sodium chloride excess in spirulina sp. (cyanobacteria). Bull Environ Contam Toxicol 2011;87:11-5.
56. Jayashree S, Thangaraju N, Gnanadoss JJ. Toxic effects of chromium on the aquatic cyanobacterium Oscillatoria sp. and removal of chromium by biosorption. J Exp Sci 2012;3(5):28-34.
57. Sultan P, Williams Shah MI, Arif Jan P, Ahamad N. Biochemical basis of heavy metal induced stress tolerance in the N2 fixing Cyanobacterium Anabaena doliolum. Afr J Cln Exper Microbiol 2007;8:8-22.
58. Khan UA, Iffat ZA. Alterations in antioxidative defense system of anabaena variabilis in the presence of heavy metals. APCBEE Procedia 2013;5:491-6.
59. Shukla MK, Tripathi RD, Sharma N, Dwivedi S, Mishra S, Singh R, et al. Responses of cyanobacterium Anabaena doliolum during nickel stress. J Environ Biol 2009;30(5):871-6.
60. Singh PK, Rai S, Pandey S, Agrawal C, Shrivastava AK. Kumar S, Rai LC. Cadmium and UV-B induced changes in proteome and some biochemical attributes of Anabaena sp. PCC7120. Phykos 2012;42(1):39-50.
61. Visviki I, Rachlin JW. The toxic action and interactions of copper and cadmium to the marine alga Dunaliella minuta in both acute the chronic exposure. Arch Environ Contam Toxicol 1991;2:271â€“5.
62. Mallick N, Mohn FH. Reactive oxygen species: response of algal cells. J Plant Physiol 2000;157:183-93.
63. Klotz LO. Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen. Biol Chem 2002;383:443â€“56.
64. Apel K, Hirt H. Reactive oxygen species: metabolism oxidative stress and signal transduction. Annu Rev Plant Biol 2004;55:373â€“99.
65. Navrot N, Rouhier N, Gelhaye E, Jaquot JP. Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant 2007;129:185-95.
66. Wise RR, Naylor AW. Chilling-enhanced photooxidation. Evidence for the role of singlet oxygen and superoxide in the breakown of pigments and endogenous antioxidants. Plant Physiol 1987;83:278-82.
67. Moller IM. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Mol Biol 2001;52:561-91.
68. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010;48:909-30.
69. Alscher RG, Donahue JL, Cramer CL. Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 1997;100(2):224-33.
70. Smirnoff N. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 1993;125:27-58.
71. Weckx JEJ, Clijsters H. Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol Plant 1996;96:506-12.
72. Meneguzzo S, Navari-Izzo F, Izzo R. Antioxidative responses of shoots and roots of wheat to increasing NaCl concentrations. J Plant Physiol 1999;155:274-80.
73. Doke N, Miura Y, Leandro MS, Kawakita K. Involvement of superoxide in signal transduction: responses to attack by pathogens, physical and chemical shocks and UV-irradiation. In: Foyer CH, Mullineaux P (eds) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. CRC Press Inc, Boca Raton, Fl; 1994. p. 177-97.
74. Murphy TM, Huerta AJ. Hydrogen peroxide formation in cultured rose cells in response to UV-C radiation. Physiol Plant 1990;78:247-53.
75. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002;7:405-10.
76. Gratao PL, Polle A, Lea PJ, Azevedo RA. Making the life of heavy metal stressed plants a little easier. Funct Plant Biol 2005;32:481-94.
77. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine, third ed. Oxford University Press, New York; 1999.
78. Garg N, Manchanda G. ROS generation in plants: boon or bane? Plant Biosys 2009;143:8-96.
79. Heath RL, Packer L. Photoperoxidation in isolated chloroplasts: kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 1968;125:180-98.
80. Luximon Ramma A, Bahorun T, Soobrattee M, Aruoma OI. Antioxidant activities of phenolic, proanthocyanidin and flavonoid components in extracts of Cassia fistula. J Agric Food Chem 2002;50:5042â€“7.
81. Giannopolitis CN, Ries SK. Superoxide dismutase: occurrence in higherplants. Plant Physiol 1977;59:309-14.
82. Zutshi S, Bano F, Ningthoujam M, Habib K, Fatma T. Metabolic adaptations to arsenic-induced oxidative stress in hapalosiphon fontinalis-339. Int J Inn Res Sci Eng Technol 2014;3(2):9386-94.
83. Hanaa H, Abd El-Baky, FKE Baz, Gamal S. El-Baroty: enhancement of antioxidant production in spirulina plantensis under oxidative stress. Am Eur J Sci Res 2007;2(2):170-9.
84. Kaiser W. The effect of hydrogen peroxide on C02 fixation of isolated intact chloroplasts. Biochim Biophys Acta 1976;440:476-82.
85. Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodriguez Serrano M, Rio LAD, et al. Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 2006;170:43-52.
86. Creissen G, Edwards A, Mullineaux P. Glutathione reductase and ascorbate peroxidase. In: Foyer CH, Mullineaux P (eds) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. CRC Press Inc, Boca Raton, Fl; 1994. p. 344-64.
87. Edwards EA, Rawsthorne S, Mullineaux PM. Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 1990;180:278-84.
88. Chalapathi Rao ASV, Reddy AR. Glutathione reductase: a putative redox regulatory system in plant cells. in: NA Khan, S Singh, S Umar (Eds.), Sulfur Assimilation and Abiotic Stresses in Plants. Springer, The Netherlands; 2008. p. 111-47.
89. Reddy AR, Raghavendra AS. Physiology and Molecular Biology of Stress Tolerance in Plants. Springer, The Netherlands; 2006. p. 157-86.
90. Szarka A, Horemans N, Kovacs Z, Grof P, Mayer M, Banhegyi G. Dehydroascorbate reduction in plant mitochondria is coupled to the respiratory electron transfer chain. Physiol Plant 2007;129:225-32.
91. Noctor G, Foyer CH. A re-evaluation of the ATP: NADPH budget during C3 photosynthesis. A contribution from nitrate assimilation and its associated respiratory activity? J Exp Bot 1998;49:1895-908.
92. Mittler R, Zilinskas BA. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J Biol Chem 1992;267:21802-7.
93. Jimenez A, Hernandez JA, Pastori G, Rio LAD, Sevilla F. Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 1998;118:1327-35.
94. Xiang C, Werner BL, Christensen EM, Oliver DJ. The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 2001;126:564-74.
95. Foyer CH, Halliwell B. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 1976;133:21â€“5.
96. Meyer AJ. The integration of glutathione homeostasis and redox signaling. J Plant Physiol 2008;165:1390-403.
97. Briviba K, Klotz LO, Sies H. Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. J Biol Chem 1997;378:1259-65.
98. Larson RA. The antioxidants of higher plants. Phytochem 1988;27:969-78.
99. Sieferman-Harms D. The light harvesting function of carotenoids in photosynthetic membrane. Plant Physiol 1987;69:561-8.
100. Collins A. Carotenoids and genomic stability. Mutat Res 2001;475:1-28.
101. Gill SS, Khan NA, Anjum NA, Tuteja N. Amelioration of cadmium stress in crop plants by nutrients management: morphological, physiological and biochemical aspects. Plant Stress (Spl issue); 2010(in press).
102. Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Bjorkman O. Photoprotection in a zeaxanthin-and lutein-deficient double mutant of Arabidopsis. Photosynth Res 2001;67:139-45.
103. Ahmad I, Hellebust A. The relationship between inorganic nitrogen metabolism and proline accumulation in osmoregulatory responses of two euryhaline microalgae. Plant Physiol 1988;88(2):348â€“54.
104. Laliberte G, Hellebust JA. Regulation of proline content of Chlorella autopica in response to change in salinity. Can J Bot 1989;67:1959â€“65.
105. Nikolopoulos D, Manetas Y. Compatible solutes and in vitro stability of Salsola soda enzyme: proline incompability. Phytochem 1991;30:411â€“3.
106. Kadpal RP, Rao NA. Alteration in the biosynthesis of proteins and nucleic acid in finger millet (Eleucine coracana) seedling during water stress and the effect of proline on protein biosynthesis. Plant Sci 1985;40:73â€“9.
107. Venekemp JH. Regulation of cytosolic acidity in plants under condition of drought. Plant Physiol 1989;76:112â€“7.
108. Smirnoff N, Cumbes QJ. Hydroxyl radical scavenging activity of compatible solutes. Phytochem 1989;28:1057-60.
109. Ashraf M, Foolad MR. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Env Exp Bot 2007;59:206-16.
110. Trovato M, Mattioli R, Costantino P. Multiple roles of proline in plant stress tolerance and development. Rendiconti Lincei 2008;19:325-46.