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High Light Intensity Augments Mercury Toxicity in Cyanobacterium Nostoc muscorum

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Abstract

The present study is aimed at investigating the role of growth irradiance in determining the extent of mercury (Hg) toxicity on various physiological parameters viz. growth, pigment contents, photosynthesis, respiration, 14CO2 fixation, photosynthetic electron transport, photorespiration and enzyme activity of cyanobacterium Nostoc muscorum. A general decline was observed in all these parameters with increasing concentration of Hg except for carotenoids content and respiratory activity which exhibited significant enhancement. This effect was more pronounced in high light (130 μmol photon m−2 s−1) exposed cells as compared to normal (70 μmol photon m−2 s−1) and low (10 μmol photon m−2 s−1) light exposed cells. Among the photosynthetic electron transport activities, whole chain was found to be more sensitive than photosystem II (PSII) and photosystem I (PSI). 14CO2 fixation was more affected as compared to O2 evolution when exposed to Hg and different light intensities. Photorespiratory activity, which is an index of protecting organisms from light-induced damage, also showed a similar declining trend. Enzyme assay revealed that among the carboxylating enzymes, activity of RUBISCO was more severely inhibited than PEPCase. Thus, these results suggest that Hg itself was toxic at all tested concentrations and high light intensity augmented its toxicity in N. muscorum inhibiting the growth, pigment contents and photosynthetic activity of the organism.

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References

  1. Nedelkoska TV, Doran PM (2000) Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnol Bioeng 67:607–615

    Article  PubMed  CAS  Google Scholar 

  2. Macfarlane GR, Burchett MD (2001) Photosynthetic pigments and peroxidase activity as indicator of heavy metal stress in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 42:233–240

    Article  PubMed  CAS  Google Scholar 

  3. Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422

    Article  Google Scholar 

  4. Halder A, Patra M, De M (2005) Evaluation of mercury toxicity by some cytological indices in leucocyte cultures. Ind J Exp Biol 43:737–739

    CAS  Google Scholar 

  5. Wang Q, Kim D, Dionysiou DD, Sorial GA, Timberlake D (2004) Sources and remediation for mercury contamination in aquatic systems—a literature review. Environ Pollut 131:323–336

    Article  PubMed  CAS  Google Scholar 

  6. Ali MB, Vajpayee P, Tripathi RD, Rai UN, Kumar A, Singh N, Behl HM, Singh SP (2000) Mercury bioaccumulation induces oxidative stress and toxicity to submerged macrophyte Potamogeton crispus L. Bull Environ Contam Toxicol 65:573–582

    Article  PubMed  CAS  Google Scholar 

  7. Murthy SDS, Sabat SC, Mohanty P (1989) Mercury-induced inhibition of photosystem II activity and changes in the emission of fluorescence from phycobilisomes in intact cells of the cyanobacterium, Spirulina platensis. Plant Cell Physiol 30:1153–1157

    CAS  Google Scholar 

  8. Matorin DN, Osipov VA, Seifullina NK, Venediktov PS, Rubin AB (2009) Increased toxic effect of methylmercury on Chlorella vulgaris under high light and cold stress conditions. Microbiology 78:321–327

    Article  CAS  Google Scholar 

  9. Dudkowiak A, Olejarz B, Lukasiewicz J, Banaszek J, Sikora J, Wiktorowicz K (2011) Heavy metals effect on cyanobacteria Synechocyctis aquatilis study using absorption, fluorescence, flow cytometry, photothermal measurements. Int J Thermophys 32:762–773

    Article  CAS  Google Scholar 

  10. Zeller S, Feller U (1999) Long-distance transport of cobalt and nickel in maturing wheat. Eur J Agron 10:91–98

    Article  CAS  Google Scholar 

  11. Murthy SDS, Mohanty P (1993) Mercury ions inhibit photosynthetic electron transport at multiple sites in the cyanobacterium Synechococcus 6301. J Biosci 18–3:355–360

    Article  Google Scholar 

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

    Google Scholar 

  13. De Filippis LF, Pallaghy CK (1992) Heavy metals: sources and biological effects. In: Rai LC, Gaur JP (eds) Phycological perspectives of water pollution. Schweizerbart, Stuttgart

    Google Scholar 

  14. Lu C, Zhang J (2000) Role of light in the response of PSII photochemistry to salt stress in the cyanobacterium Spirulina platensis. J Exp Bot 51–346:911–917

    Article  Google Scholar 

  15. Lupi FM, Fernandes HML, Sá-Correia I (1998) Increase of copper toxicity to growth of Chlorella vulgaris with increase of light intensity. Microbiol Ecol 35–2:193–198

    Article  Google Scholar 

  16. Baker NR, Fernyhough P, Meek IT (2006) Light dependent inhibition of photosynthetic electron transport by zinc. Physiol Plant 56–2:217–222

    Google Scholar 

  17. Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    Article  PubMed  CAS  Google Scholar 

  18. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Ann Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  CAS  Google Scholar 

  19. Gerloff GC, Fitzgerald GP, Skoog F (1950) The isolation, purification and culture of blue-green algae. Am J Bot 37:216–218

    Article  CAS  Google Scholar 

  20. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  21. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents; verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  22. Goodwin TW (1954) Carotenoids. In: Paech K, Tracey MV (eds) Handbook of plant analysis, vol 3. Springer, Berlin, pp 272–311

    Google Scholar 

  23. Blumwald E, Tel-Or E (1982) Structural aspects of the Nostoc muscorum to salt. Arch Microbiol 132:163–167

    Article  CAS  Google Scholar 

  24. Prasad SM, Zeeshan M (2004) Effect of UV-B and monocrotophos, singly and in combination, on photosynthetic activity and growth of non-heterocystous cyanobacterium Plectonema boryanum. Environ Exp Bot 52:175–184

    Article  CAS  Google Scholar 

  25. Zelitch I (1968) Investigations on photorespiration with sensitive 14C-assay. Plant Physiol 43:1829–1837

    Article  PubMed  CAS  Google Scholar 

  26. Spiller H (1980) Photophosphorylation capacity of stable spheroplasts preparations of Anabaena. Plant Physiol 66:446–450

    Article  PubMed  CAS  Google Scholar 

  27. Codd GA, Stewart WDP (1977) D-Ribulose-1, 5-diphosphate carboxylase from the blue-green alga Aphanocapsa 6308. Arch Microbiol 113:105–110

    Article  CAS  Google Scholar 

  28. Raghavendra AS, Das VSR (1975) Malonate-inhibition of allosteric PEP carboxylase from Setaria italica. Biochem Biophys Res Commun 66:160–165

    Article  PubMed  CAS  Google Scholar 

  29. De Lorimier RM, Smith RL Jr, Stevens SE (1992) Regulation of phycobilisome structure and gene expression by light intensity. Plant Physiol 98:1003–1010

    Article  PubMed  Google Scholar 

  30. Wherley BG, Gardner DS, Metzger JD (2005) Tall fescue photomorphogenesis as influenced by changes in the spectral composition and light intensity. Crop Sci 45:562–568

    Article  Google Scholar 

  31. Zengin FF, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Ser Bot 47–2:157–164

    Google Scholar 

  32. Vavillin DV, Polynov VA, Matorin DN, Venediktov PS (1995) Sublethal concentrations of copper stimulate photosystem II: photoinhibition in Chlorella pyrenoidosa. J Plant Physiol 146:609–614

    Article  Google Scholar 

  33. Prasad SM, Zeeshan M (2005) Ultraviolet-B and cadmium, alone and together, induced changes in growth, photosynthesis and antioxidant enzymes of cyanobacterium Plectonema boryanum. Biol Plant 49–2:1–7

    Google Scholar 

  34. Singh CB, Singh SP (1992) Protective effects of Ca2+, Mg2+, Cu2+, and Ni2+ on mercury and methylmercury toxicity to a cyanobacterium. Ecotoxicol Environ Saf 23:1–10

    Article  PubMed  CAS  Google Scholar 

  35. Choudhari 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 Saf 66:204–209

    Article  CAS  Google Scholar 

  36. Kupper H, Kupper F, Spiller M (1996) Environmental relevance of heavy metal substituted chlorophylls using the example of water plants. J Exp Bot 47:259–266

    Article  Google Scholar 

  37. Solymosi K, Lenti K, Mysliwa-Kurdziel B, Fidy J, Strzalka K, Boddi B (2004) Depending on concentration, Hg2+ reacts with different components of the NADPH: protochlorophyllide oxidoreductase macrodomains. Plant Biol 6:358–363

    Article  PubMed  CAS  Google Scholar 

  38. Janik E, Grudzinski W, Gruszecki WI, Krupa Z (2008) The xanthophylls cycle pigments in Secale cereale leaves under combined cadmium and high light stress conditions. J Photochem and Photobiol B 90–1:47–52

    Article  CAS  Google Scholar 

  39. Kobayashi JS, Kakizono T, Nishio N, Nagai S, Kurimara Y, Tsuji Y (1997) Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Appl Microbiol Biotechnol 48:351–356

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  41. Mallick N (2004) Copper-induced oxidative stress in the chlorophycean microalga Chlorella vulgaris: response of the antioxidant system. J Plant Physiol 161:591–597

    Article  PubMed  CAS  Google Scholar 

  42. Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193

    Article  CAS  Google Scholar 

  43. Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32:327–347

    Article  CAS  Google Scholar 

  44. De Fillipis LF, Zeigler H (1993) Effect of sublethal concentrations of zinc, cadmium and mercury on the photosynthetic carbon reduction cycle of Euglena. J Plant Physiol 142:167–172

    Article  Google Scholar 

  45. Lu CM, Chau CW, Zhang JH (2000) Acute toxicity of excess mercury on the photosynthetic performance of cyanobacterium, Spirulina platensis—assessment by chlorophyll fluorescence analysis. Chemosphere 41:191–196

    Article  PubMed  CAS  Google Scholar 

  46. Bazzaz MB, Govindjee (1974) Effects of cadmium nitrate on spectral characteristics and light reaction of chloroplasts. Environ Lett 6:1–12

    Article  PubMed  CAS  Google Scholar 

  47. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  PubMed  CAS  Google Scholar 

  48. Chow WS, Aro EM (2006) Photoinactivation and mechanisms of recovery photosystem II. In: Wydrzynski T, Satoh K (eds) The light-driven water: plastoquinone oxidoreductase. Springer, Dordecht, pp 627–648

    Google Scholar 

  49. Van Assche F, Clijsters H (1990) Effect of metals on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  50. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  51. Devine M, Duke SO, Fedtke C (1993) Physiology of herbicide action. Prentice Hall, Englewood Cliffs

    Google Scholar 

  52. Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. Biochim Biophys Acta 1708–3:352–361

    Google Scholar 

  53. Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50

    Article  PubMed  CAS  Google Scholar 

  54. Singh R, Srivastava PK, Singh VP, Dubey G, Prasad SM (2011) Light intensity determines the extent of mercury toxicity in the cyanobacterium Nostoc muscorum. Acta Physiol Plant. doi:10.1007/s11738-011-0909-3

  55. Rai LC, Tyagi B, Mallick N, Rai PK (1995) Interactive effects of UV-B and copper on photosynthetic activity of the cyanobacterium Anabaena doliolum. Environ Exp Bot 35:177–185

    Article  CAS  Google Scholar 

  56. Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage repair cycle of photosystem II in Synechocystis sp. PCC6803. Biochim Biophys Acta 1657–1:23–32

    Google Scholar 

  57. Subrahmanyam D, Rathore VS (2000) Influence of manganese toxicity on photosynthesis in ricebean (Vigna umbellata) seedlings. Photosynthetica 38:449–453

    Article  CAS  Google Scholar 

  58. Matoo AK, Marder JB, Edelman M (1989) Dynamics of the photosystem II reaction centre. Cell 56:241–246

    Article  Google Scholar 

  59. Ouzounidou G, Moustakas M, Symeonidis L, Karataglis S (2006) Response of wheat seedlings to Ni stress: effects of supplemental calcium. Arch Environ Contam Toxicol 50:346–352

    Article  PubMed  CAS  Google Scholar 

  60. Jiang H, Qiu B (2011) Inhibition of photosynthesis by UV-B exposure and its repair in the bloom-forming cyanobacterium Microcystis aeruginosa. J Appl Phycol 23:691–696

    Article  CAS  Google Scholar 

  61. Passow H, Rathstein A, Clarkson TW (1961) The general pharmacology of heavy metals. Pharmacol Rev 13:185–224

    PubMed  CAS  Google Scholar 

  62. Romero-Puertas MC, Palma JM, Gómez M, Del Rio LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25–5:677–686

    Article  Google Scholar 

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Acknowledgments

The authors are thankful to The Head, Department of Botany, University of Allahabad, Allahabad, for providing necessary laboratory facilities and to the University Grants Commission, New Delhi, India, for providing grants to purchase necessary instruments for the experiments performed. The authors are also indebted to Prof. L.C. Rai, BHU, Varanasi, for giving the permission to use the liquid scintillation counter (L.K.B., Wallace 1209, Rockbeta, USA) for 14CO2 fixation experiment.

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Correspondence to Sheo Mohan Prasad.

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Singh, R., Dubey, G., Singh, V.P. et al. High Light Intensity Augments Mercury Toxicity in Cyanobacterium Nostoc muscorum . Biol Trace Elem Res 149, 262–272 (2012). https://doi.org/10.1007/s12011-012-9421-x

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  • DOI: https://doi.org/10.1007/s12011-012-9421-x

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