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Nostoc muscorum and Phormidium foveolarum differentially respond to butachlor and UV-B stress

Abstract

Present study deals with responses of two cyanobacteria viz. Nostoc muscorum and Phormidium foveolarum against butachlor [2-chloro-2,6-diethyl-N-(butoxymethyl) acetanilide] (low dose; 5 µg mL−1 and high dose; 10 µg mL−1) and UV-B (7.2 kJ m−2) alone, and in combination. Butachlor and UV-B exposure, alone and in combination, suppressed growth of both the cyanobacteria. This was accompanied by inhibitory effect on whole cell oxygen evolution and photosynthetic electron transport activities. Both the stressors induced the oxidative stress as there was significant increase in superoxide radical (O2·−) and hydrogen peroxide (H2O2) contents resulting into increased lipid peroxidation and electrolyte leakage. In N. muscorum, low dose of butachlor and UV-B alone increased the activities of superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD), while activity of all these enzymatic antioxidants declined significantly at treatments with high dose of butachlor alone, and with low and high doses of butachlor and UV-B in combination. In P. foveolarum, enhanced activity of SOD, CAT and POD (except POD at high dose of butachlor and UV-B combination) was noticed. Ascorbate level in N. muscorum declined progressively with increasing intensity of stress while in P. foveolarum varied response was noticed. Proline contents increased progressively under tested stress in both the organisms. Overall results suggest that N. muscorum was more sensitive than P. foveolarum against butachlor and UV-B stresses. Hence, P. foveolarum may be preferred in paddy field for sustainable agriculture.

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References

  1. Aktar MW, Sengupta D, Purkait S, Chowdhury A (2008) Vertical migration of some herbicides through undisturbed and homogenized soil columns. Interdiscip Toxicol 1:231–235

    PubMed  PubMed Central  Google Scholar 

  2. Alla MMN, Badawi AHM, Hassan NM, El-Bastawisy ZM, Badran EG (2007) Induction of glutathione and glutathione-associated enzymes in butachlor-tolerant plant species. Am J Plant Physiol 2:195–205

    CAS  Google Scholar 

  3. Anand N, Hopper RSSK (1987) Blue-green algae from rice fields in Kerala State, India. Hydrobiologia 144:223–232

    Google Scholar 

  4. Anderson TW (1958) An introduction to multivariate analysis. Wiley, New York

    Google Scholar 

  5. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  6. Beestman GB, Deming JM (1974) Dissipation of acetanilide herbicides from soils. Agron J 66:308–311

    CAS  Google Scholar 

  7. Bernroitner M, Zamocky M, Furtmüller PG, Peschek GA, Obinger C (2009) Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteria. J Exp Bot 60:423–440

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  9. Böger P, Matthes B, Schmalfuß J (2000) Towards the primary target of chloroacetamides: new findings pave the way. Pest Manag Sci 56:497–508

    Google Scholar 

  10. Carletti P, Masi A, Wonisch A, Grill D, Tausz M, Ferretti M (2003) Changes in antioxidants and pigment pool dimensions in UV-B irradiated maize seedlings. Environ Exp Bot 50:149–157

    CAS  Google Scholar 

  11. Chen YL, Chen CC (1979) Degradation and dissipation of herbicide butachlor. J Pestic Sci 4:431–438

    CAS  Google Scholar 

  12. Chen Z, Jauneau P, Qiu B (2007) Effects of three pesticides on the growth, photosynthesis and photoinhibition of the edible cyanobacterium Ge-Xian-Mi (Nostoc). Aquat Toxicol 81:256–265

    CAS  PubMed  Google Scholar 

  13. Chen WC, Yen JH, Chang CS, Wang YS (2009) Effects of herbicide butachlor on soil microorganisms and on nitrogen-fixing abilities in paddy soil. Ecotoxicol Environ Saf 72:120–127

    CAS  PubMed  Google Scholar 

  14. Chen L, Xie M, Bi Y, Wang G, Deng S, Liu Y (2012) The combined effects of UV-B radiation and herbicides on photosynthesis, antioxidant enzymes and DNA damage in two bloom-forming cyanobacteria. Ecotoxicol Environ Saf 80:224–230

    CAS  PubMed  Google Scholar 

  15. Das AC, Debnath A (2006) Effect of systemic herbicides on N2-fixing and phosphate solubilizing microorganisms in relation to availability of nitrogen and phosphorus in paddy soils of West Bengal. Chemosphere 65:1082–1086

    CAS  PubMed  Google Scholar 

  16. Debnath A, Das AC, Mukherjee D (2002) Persistence and effect of butachlor and basalin on the activities of phosphate solubilizing microorganisms in wetland rice soil. Bull Environ Contam Toxicol 68:766–770

    CAS  PubMed  Google Scholar 

  17. Desikachary TV (1959) Cyanophyta. Indian Council of Agricultural Research, New Delhi

    Google Scholar 

  18. Dowidar SMA, Osman MEH, El-Naggar AH, Khalefa AE (2010) Effect of butachlor and thiobencarb herbicides on protein content and profile and some enzyme activities of Nostoc muscorum. J Gen Eng Biotechnol 8:89–95

    Google Scholar 

  19. Egashira T, Takahama U, Nakamura K (1989) A reduced activity of catalase as a basis for light dependent methionine sensitivity of a Chlamydomonas reinhardtii mutant. Plant Cell Physiol 30:1171–1175

    CAS  Google Scholar 

  20. Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxyl ammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    CAS  PubMed  Google Scholar 

  21. Estevez MS, Malanga G, Puntarulo S (2001) UV-B effects on Antarctic Chlorella sp cells. J Photochem Photobiol B Biol 62:19–25

    CAS  Google Scholar 

  22. Fernandes TA, Iyer V, Apte SK (1993) Differential responses of nitrogen-fixing cyanobacteria to salinity and osmotic stresses. Appl Environ Microbiol 59:899–904

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Flint SD, Caldwell MM (2003) A biological spectral weighting function for ozone depletion research with higher plants. Physiol Plant 117:137–144

    CAS  Google Scholar 

  24. Gahagen HE, Halm RE, Abeles FB (1968) Effect of ethylene on peroxidase activity. Physiol Plant 21:1270–1279

    Google Scholar 

  25. Galhano V, Peixoto F, Gomes-Laranjo J (2010) Bentazon triggers the promotion of oxidative damage in the Portuguese rice field cyanobacterium Anabaena cylindrica: response of the antioxidant system. Environ Toxicol 25:517–526

    CAS  PubMed  Google Scholar 

  26. Galhano V, Gomes-Laranjo J, Peixoto F (2011a) Exposure of the cyanobacterium Nostoc muscorum from Portuguese rice fields to molinate (Ordram®): effects on the antioxidant system and fatty acid profile. Aquat Toxicol 101:367–376

    CAS  PubMed  Google Scholar 

  27. Galhano V, Santos H, Oliveira MM, Gomes-Laranjo J, Peixotoc F (2011b) Changes in fatty acid profile and antioxidant systems in a Nostoc muscorum strain exposed to the herbicide bentazon. Process Biochem 46:2152–2162

    CAS  Google Scholar 

  28. Gantt E, Conti SF (1966) Granules associated with the chloroplast lamellae of Porphyridium cruentum. J Cell Biol 29:423–434

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Garcia-Pichel F, Wingard CE, Castenholz RW (1993) Evidence regarding the UV sunscreen role of a mycosporine-like compound in the cyanobacterium Gloeocapsa sp. Appl Environ Microbiol 59:170–176

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Giannopolitis CN, Ries SK (1977) Superoxide dismutase occurrence in higher plants. Plant Physiol 59:309–314

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Gong M, Li YJ, Chen SZ (1998) Abscisic acid-induced thermo-tolerance in maize seedlings is mediated by calcium and associated with antioxidant system. J Plant Physiol 153:488–496

    CAS  Google Scholar 

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

    Google Scholar 

  33. Gotz T, Böger P (2004) The very-long-chain fatty acid synthase is inhibited by chloroacetamides. Z Naturforsch 59:549–553

    Google Scholar 

  34. He Y, Häder DP (2002) Reactive oxygen species and UV-B effects on cyanobacteria. Photochem Photobiol Sci 1:729–736

    CAS  PubMed  Google Scholar 

  35. He H, Li Y, Chen T, Huang X, Guo Q, Li S, Yu T, Li H (2013) Butachlor induces some physiological and biochemical changes in a rice field biofertilizer cyanobacterium. Pestic Biochem Physiol 105:224–230

    CAS  Google Scholar 

  36. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  PubMed  Google Scholar 

  37. 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

    CAS  Google Scholar 

  38. Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103

    CAS  PubMed  Google Scholar 

  39. Kumari N, Narayan OP, Rai LC (2009) Understanding butachlor toxicity in Aulosira fertilissima using physiological, biochemical and proteomic approaches. Chemosphere 77:1501–1507

    CAS  PubMed  Google Scholar 

  40. Kumari N, Narayan OP, Rai LC (2012) Cyanobacterial diversity shifts induced by butachlor in selected Indian rice fields in Eastern Uttar Pradesh and Western Bihar analyzed with PCR and DGGE. J Microbiol Biotechnol 22:1–12

    CAS  PubMed  Google Scholar 

  41. Lemoine Y, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177

    CAS  PubMed  Google Scholar 

  42. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  43. Ma J, Wang S, Wang P, Ma L, Chen X, Xu R (2006) Toxicity assessment of 40 herbicides to the green alga Raphidocelis subcapitata. Ecotoxicol Environ Saf 63:456–462

    CAS  PubMed  Google Scholar 

  44. Ma J, Tong S, Wang P, Chen J (2010) Toxicity of seven herbicides to the three cyanobacteria Anabaena flos-aquae, Microcystis flos-aquae and Mirocystis aeruginosa. Int J Environ Res 4:347–352

    CAS  Google Scholar 

  45. Martin H, Worthing CR (1974) Pesticide manual, 4th edn. British Crop Protection Council, Farnham

    Google Scholar 

  46. Matysik J, Alia BB, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  47. Müller-Moulé P, Havaux M, Niyogi KK (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol 133:748–760

    PubMed  PubMed Central  Google Scholar 

  48. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    CAS  PubMed  Google Scholar 

  49. Ohki K, Zehr PJ, Fujita Y (1992) Regulation of nitrogenase activity in relation to the light dark regime in the filamentous non-heterocystous cyanobacterium Trichodesmium sp. NIBB 1067. J Gen Appl Microbiol 138:2679–2685

    CAS  Google Scholar 

  50. Olsson LC, Fraysse L, Bornman JF (2000) Influence of high light and UV-B radiation on photosynthesis and D1 turnover in atrazine-tolerant and-sensitive cultivars of Brassica napus. J Exp Bot 51:265–274

    CAS  PubMed  Google Scholar 

  51. Oser BL (1979) Hawks physiological chemistry. McGraw Hill, New York, pp 702–705

    Google Scholar 

  52. 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  54. Prasad SM, Zeeshan M (2005) UV-B radiation and cadmium induced changes in growth, photosynthesis, and antioxidant enzymes of cyanobacterium Plectonema boryanum. Biol Plant 49:229–236

    CAS  Google Scholar 

  55. Rastogi RP, Singh SP, Hader DP, Sinha RP (2011) Ultraviolet-B-induced DNA damage and photorepair in the cyanobacterium Anabaena variabilis PCC 7937. Environ Exp Bot 74:280–288

    CAS  Google Scholar 

  56. Renger G, Volker M, Eckert HJ, Frome R, Hohm-Veit S, Graber P (1989) On the mechanism of photosystem II deterioration by UV-B irradiation. Photochem Photobiol 49:97–105

    CAS  Google Scholar 

  57. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  58. Sagisaka S (1976) The occurrence of peroxide in a perennial plant Populas gelrica. Plant Physiol 57:308–309

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Sheeba SV, Srivastava PK, Prasad SM (2011) Differential physiological and biochemical responses of two cyanobacteria Nostoc muscorum and Phormidium foveolarum against oxyfluorfen and UV-B radiation. Ecotoxicol Environ Saf 74:1981–1993

    CAS  PubMed  Google Scholar 

  60. Singh S, Datta P (2006) Screening and selection of most potent diazotrophic cyanobacterial isolate exhibiting natural tolerance to rice field herbicides for exploitation as biofertilizer. J Basic Microbiol 46(3):191–225

    Google Scholar 

  61. Singh S, Datta P, Tirkey A (2011) Response of multiple herbicide resistant strain of diazotrophic cyanobacterium Anabaena variabilis exposed to atrazine and DCMU. Ind J Exp Biol 49:298–303

    Google Scholar 

  62. Singh DP, Khattar JS, Kaur K, Sandhu BS, Singh Y (2012a) Toxicological impact of anilofos on some physiological processes of a rice field cyanobacterium Anabaena torulosa. Toxicol Environ Chem 94:1304–1318

    CAS  Google Scholar 

  63. Singh S, Datta P, Tirkey A (2012b) Isolation and characterization of a multiple herbicide resistant strain [Av(MHR)Ar, Al, B, D] of diazotrophic cyanobacterium Anabaena variabilis. Ind J Biotechnol 11:77–85

    CAS  Google Scholar 

  64. Singh VP, Srivastava PK, Prasad SM (2012c) Impact of low and high fluence rates of UV-B radiation on growth and oxidative stress in Phormidium foveolarum and Nostoc muscorum under copper toxicity: differential display of antioxidants system. Acta Physiol Plant 34:2225–2239

    CAS  Google Scholar 

  65. Singh VP, Srivastava PK, Prasad SM (2012d) Differential effects of UV-B radiation fluence rates on growth, photosynthesis and phosphate metabolism in two cyanobacteria under copper toxicity. Toxicol Environ Chem 94:1511–1535

    CAS  Google Scholar 

  66. Singh VP, Srivastava PK, Prasad SM (2012e) Differential effect of UV-B radiation on growth, oxidative stress and ascorbate-glutathione cycle in two cyanobacteria under copper toxicity. Plant Physiol Biochem 61:61–70

    CAS  PubMed  Google Scholar 

  67. Singh DP, Khattar JIS, Kaur M, Kaur G, Gupta M, Singh Y (2013) Anilofos tolerance and its mineralization by the cyanobacterium Synechocystis sp. strain PUPCCC 64. PLoS ONE 8(1):e53445. https://doi.org/10.1371/journal.pone.0053445

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. Sinha RP, Singh N, Kumar A, Kumar AD, Häder H, Häder DP (1996) Effects of UV irradiation on certain physiological and biochemical process in cyanobacteria. Photochem Photobiol 32:311–314

    Google Scholar 

  69. Sinha RP, Klisch M, Helbling EW, Häder D (2001) Induction of mycosporine-like amino acids (MAAs) in cyanobacteria by solar ultraviolet-B radiation. J Photochem Photobiol, B 60:129–135

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Srivastava PK, Singh VP, Prasad SM (2012) Compatibility of ascorbate-glutathione cycle enzymes in cyanobacteria against low and high UV-B exposures, simultaneously exposed to low and high doses of chlorpyrifos. Ecotoxicol Environ Saf 83:79–88

    CAS  PubMed  Google Scholar 

  72. Thakkar M, Randhawa V, Wei L (2013) Comparative responses of two species of marine phytoplankton to metolachlor exposure. Aquat Toxicol 126:198–206

    CAS  PubMed  Google Scholar 

  73. Tiwari DN, Kumar A, Mishra AK (1991) Use of cyanobacterial diazotrophic technology in rice agriculture. Appl Biochem Biotechnol 28–29:387–396

    Google Scholar 

  74. Ueji M, Inao K (2001) Rice paddy field herbicides and their effects on the environment and ecosystems. Weed Biol Manag 1:71–79

    CAS  Google Scholar 

  75. Vaishampayan A (1985) Mutagenic activity of alachlor, butachlor and carbaryl to a N2-fixing cyanobacterium Nostoc muscorum. J Agric Sci 104:571–576

    CAS  Google Scholar 

  76. Vaishampayan A, Sinha RP, Hader DP, Dey T, Gupta AK, Bhan U, Rao AL (2001) Cyanobacterial biofertilizers in rice agriculture. Bot Rev 67:453–516

    Google Scholar 

  77. Wang YR, Liu CW, Niu CY, Cai LB, Li ZX, Zhu CS, He SJ, Wang QS (1996) Phototransformation of butachlor in aquatic system and its fate in rice fields. Acta Sci Circ 16:475–481

    CAS  Google Scholar 

  78. Wang G, Deng S, Li C, Liu Y, Chen L, Hu C (2012) Damage to DNA caused by UV-B radiation in the desert cyanobacterium Scytonema javanicum and the effects of exogenous chemicals on the process. Chemosphere 88:413–417

    CAS  PubMed  Google Scholar 

  79. Wang J, Wu G, Chen L, Zhang W (2013a) Cross-species transcriptional network analysis reveals conservation and variation in response to metal stress in cyanobacteria. BMC Genom 14:112. https://doi.org/10.1186/1471-2164-14-112

    CAS  Article  Google Scholar 

  80. Wang S, Li H, Lin C (2013b) Physiological, biochemical and growth responses of Italian rye grass to butachlor exposure. Pestic Biochem Physiol 106:21–27

    CAS  Google Scholar 

  81. Wilson A, Ajlani G, Verbavatz JM, Vassc I, Kerfeldd CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Xie Z, Wang Y, Liu Y, Liu Y (2009) Ultraviolet-B exposure induces photo-oxidative damage and subsequent repair strategies in a desert cyanobacterium Microcoleus vaginatus Gom. Eur J Soil Biol 45:377–382

    CAS  Google Scholar 

  83. Yu YL, Chen YX, Luo YM, Pan XD, He YF, Wong MH (2003) Rapid degradation of butachlor in wheat rhizosphere soil. Chemosphere 50:771–774

    CAS  PubMed  Google Scholar 

  84. Zhao S, Pan WB, Ma C (2012) Stimulation and inhibition effects of algae-lytic products from Bacillus cereus strain L7 on Anabaena flos-aquae. J Appl Phycol 24:1015–1021

    CAS  Google Scholar 

  85. Zheng HH, Ye CM (2001) Identification of UV photoproducts and hydrolysis products of butachlor by mass spectrometry. Environ Sci Technol 35:2889–2895

    CAS  PubMed  Google Scholar 

  86. Zhou Z, Yang Z, Li Y (2012) Effect of CO2 increase in atmosphere and UV-B intensification on Nostoc commune photosynthetic pigment and UV-B masking materials. Wuhan Univ J Nat Sci 17:255–260

    CAS  Google Scholar 

  87. Zhu Y, Graham JE, Ludwig M, Xiong W, Alvey RM, Shen G, Bryant DA (2010) Roles of xanthophyll carotenoids in protection against photoinhibition and oxidative stress in the cyanobacterium Synechococcus sp. strain PCC 7002. Arch Biochem Biophys 504:86–99

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are thankful to The Head, Department of Botany, University of Allahabad, Allahabad for providing necessary laboratory facilities. The authors are also thankful to University Grants Commission, New Delhi for providing financial support to carry out this work.

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Sheeba, Ruhil, K. & Prasad, S.M. Nostoc muscorum and Phormidium foveolarum differentially respond to butachlor and UV-B stress. Physiol Mol Biol Plants 26, 841–856 (2020). https://doi.org/10.1007/s12298-019-00754-5

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Keywords

  • Butachlor
  • Cyanobacteria
  • Differential sensitivity
  • Oxidative stress
  • Photosynthesis
  • UV-B radiation