Advertisement

Ecotoxicology

, Volume 20, Issue 2, pp 337–347 | Cite as

Bioaccumulation and degradation of pesticide fluroxypyr are associated with toxic tolerance in green alga Chlamydomonas reinhardtii

  • Shuang Zhang
  • Chong Bin Qiu
  • You Zhou
  • Zhen Peng Jin
  • Hong Yang
Article

Abstract

The herbicide fluroxypyr is widely used for controlling weeds and insects but intensive use of fluroxypyr has resulted in its widespread contamination in soils and aquatic ecosystems. To evaluate the eco-toxicity of fluroxypyr to green algae, bioaccumulation and degradation of fluroxypyr in Chlamydomonas reinhardtii, a model unicellular alga, along with its biological adaptation to fluroxypyr toxicity were investigated. The microalgae were treated with fluroxypyr at 0.05–1.00 mg l−1 for 2 days or 0.50 mg l−1 for 1–5 days. The growth of C. reinhardtii was stimulated at low levels of fluroxypyr (0.05–0.5 mg l−1) but inhibited at high concentrations (0.75–1.00 mg l−1). Fluroxypyr was significantly accumulated by C. reinhardtii. Interestingly, the accumulated fluroxypyr could be rapidly degraded in the cells. On day 5 more than 57% of cellular fluroxypyr was degraded. Our results indicated that accumulation and degradation of fluroxypyr occurred simultaneously. Treatment with 0.05–1.00 mg l−1 fluroxypyr for 30 min induced significant production of reactive oxygen species and as a consequence resulted in accumulation of peroxides and DNA degradation. Additionally, activities of several major antioxidant enzymes were activated in C. reinhardtii exposed to high levels of fluroxypyr. Overall, the present studies represent the initial comprehensive analyses of the green alga C. reinhardtii in adaptation to the fluroxypyr-contaminated aquatic ecosystems.

Keywords

Fluroxypyr Bioaccumulation Biodegradation Chlamydomonas reinhardtii Oxidation 

Notes

Acknowledgments

The authors acknowledge the financial support of the Fundamental Research Funds for the Central Universities of China (No. KYZ200918) and the National Natural Science Foundation of China (No. 21077055) for this study.

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  2. Affenzeller MJ, Darehshouri A, Andosch A, Lütz C, Lütz-Meindl U (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Bot 60:939–954CrossRefGoogle Scholar
  3. Albanis TA, Danis TG, Kourgia MK (1994) Transportation of pesticides in estuaries of the Axios, Loudias and Aliakmon rivers (Thermaikos Gulf), Greece. Sci Total Environ 156:11–22CrossRefGoogle Scholar
  4. Arias-Estévez M, López-Periago E, Martínez-Carballo E, Simal-Gándara J, Mejuto JC, García-Río L (2008) The mobility and degradation of pesticides in soils and the pollution of groundwater resources. Agric Ecosyst Environ 123:247–260CrossRefGoogle Scholar
  5. Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu JL, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143:312–325CrossRefGoogle Scholar
  6. Beauchamp C, Fridovixh I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefGoogle Scholar
  7. Cedergreen N, Andersen L, Olesen CF, Spliid HH, Streibig JC (2005) Does the effect of herbicide pulse exposure on aquatic plants depend on K ow or mode of action. Aquat Toxicol 71:261–271CrossRefGoogle Scholar
  8. Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzè D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795CrossRefGoogle Scholar
  9. De Gara L, Locato V, Dipierro S, De Pinto MC (2010) Redox homeostasis in plants. The challenge of living with endogenous oxygen production. Respir Physiol Neurobiol 173(Suppl):S13–S19CrossRefGoogle Scholar
  10. DeLorenzo ME, Taylor LA, Lund SA, Pennington PL, Strozier ED, Fulton MH (2002) Toxicity and bioconcentration potential of the agricultural pesticide endosulfan in phytoplankton and zooplankton. Arch Environ Contam Toxicol 42:173–181CrossRefGoogle Scholar
  11. Elbaz A, Wei YY, Meng Q, Zheng Q, Yang ZM (2010) Mercury-induced oxidative stress and impact on antioxidant enzymes in Chlamydomonas reinhardtii. Ecotoxicology 19:1285–1293CrossRefGoogle Scholar
  12. Fatokio S, Awofolu OR (2004) Levels of organochlorine pesticide residues in marine-, surface-, ground-, and drinking waters from the Eastern Cape Province of South Africa. J Environ Sci Health Part B 39:101–114CrossRefGoogle Scholar
  13. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferase: the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  14. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322CrossRefGoogle Scholar
  15. Hela DG, Lambropoulou DA KKA, Albanis TA (2005) Environmental monitoring and ecological risk assessment for pesticide contamination and effects in Lake Pamvotis, northwestern Greece. Environ Toxicol Chem 24:1548–1556CrossRefGoogle Scholar
  16. Hiltonen T, Clarke AK, Karlsson J, Samuelsson G (1996) A cDNA coding for glutathione S-transferase from the unicellular green algae Coccomyxa sp. Gene 176:263–264CrossRefGoogle Scholar
  17. Hong Y, Hu HY, Li FM (2008) Growth and physiological responses of freshwater green alga Selenastrum capricornutum to allelochemical ethyl 2-methyl acetoacetate (EMA) under different initial algal densities. Pestic Biochem Physiol 90:203–212CrossRefGoogle Scholar
  18. Jain M, Ghanashyam C, Bhattacharjee A (2010) Comprehensive expression analysis suggests overlapping and specific roles of rice glutathione S-transferase genes during development and stress responses. BMC Genomics 11:73CrossRefGoogle Scholar
  19. Jiang L, Yang H (2009) Prometryne-induced oxidative stress and impact on antioxidant enzymes in wheat. Ecotoxicol Environ Saf 72:1687–1693CrossRefGoogle Scholar
  20. Jonsson CM, Aoyama H (2007) In vitro effect of agriculture pollutants and their joint action on Pseudokirchneriella subcapitata acid phosphatase. Chemosphere 69:849–855CrossRefGoogle Scholar
  21. Li R, Chen GZ, Tam NFY, Luan TG, Shin PKS, Cheung SG, Liu Y (2009) Toxicity of bisphenol A and its bioaccumulation and removal by a marine microalga Stephanodiscus hantzschii. Ecotoxicol Environ Saf 72:321–328CrossRefGoogle Scholar
  22. Liebig M, Schmidt G, Bontje D, Kooi BW, Streck G, Traunspurger W, Knacker T (2008) Direct and indirect effects of pollutants on algae and algivorous ciliates in an aquatic indoor microcosm. Aquat Toxicol 88:102–110CrossRefGoogle Scholar
  23. Liu HJ, Xiong MY (2009) Comparative toxicity of racemic metolachlor and S-metolachlor to Chlorella pyrenoidosa. Aquat Toxicol 93:100–106CrossRefGoogle Scholar
  24. Liu Y, Luan TG, Lu NN, Lan CY (2006) Toxicity of fluoranthene and its biodegradation by Cyclotella caspia alga. J Integrative Plant Biol 48:169–180CrossRefGoogle Scholar
  25. Ma J (2002) Differential sensitivity to 30 herbicides among populations of two green algae Scenedesmus obliquus and Chlorella pyrenoidosa. Bull Environ Contam Toxicol 68:275–281Google Scholar
  26. Ma JY, Zheng RQ, Xu LG, Wang SF (2002) Differential sensitivity of two green algae, Scenedesmus obliqnus and Chlorella pyrenoidosa, to 12 pesticides. Ecotoxicol Environ Saf 52:57–61CrossRefGoogle Scholar
  27. Mendez-Alvarez S, Leisinger U, Eggen RIL (1999) Adaptive responses in Chlamydomonas reinhardtii. Int Microbiol 2:15–22Google Scholar
  28. Mittler R (2002) Oxidative stress, antioxidants and stress to tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  29. Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue terazolium. Anal Biochem 212:540–546CrossRefGoogle Scholar
  30. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  31. Prado R, García R, Rioboo C, Herrero C, Abalde J, Cid A (2009a) Comparison of the sensitivity of different toxicity test endpoints in a microalga exposed to the herbicide paraquat. Environ Int 35:240–247CrossRefGoogle Scholar
  32. Prado R, Rioboo C, Herrero C, Cid A (2009b) The herbicide paraquat induces alterations in the elimental and biochemical composition of non-target microalgal species. Chemosphere 76:1440–1444CrossRefGoogle Scholar
  33. Qian HF, Chen W, Li JJ, Wang J, Zhou Z, Liu WP, Fu ZW (2009) The effect of exogenous nitric oxide on alleviating herbicide damage in Chlorella vulgaris. Aquat Toxicol 92:250–257CrossRefGoogle Scholar
  34. Ross C, Santiago-Vázquez L, Paul V (2006) Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 78:66–73CrossRefGoogle Scholar
  35. Slater AFG, Nobel CSI, Orrenius S (1995) The role of intracellular oxidants in apoptosis. Biochim Biophys Acta 1271:59–62Google Scholar
  36. Song NH, Yin XL, Chen GF, Yang H (2007) Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere 68:1779–1787CrossRefGoogle Scholar
  37. Song NH, Zhang S, Hong M, Yang H (2010) Impact of dissolved organic matter on bioavailability of chlorotoluron to wheat. Environ Pollut 158:906–912CrossRefGoogle Scholar
  38. Steen RJCA, Leonards PEG, Brinkman UAT, Barcelo D, Tronczynski J, Albanis TA, Cofino WP (1999) Ecological risk assessment of agrochemicals in European estuaries. Environ Toxicol Chem 18:1574–1581CrossRefGoogle Scholar
  39. Tao L, Yang H (2010) Fluroxypyr biodegradation in soils by multiple factors. Environ Monit Assess. doi: 10.1007/s10661-010-1508-2
  40. Tao L, Wu GL, Zhang R, Chen G, Cui J, Yang H (2009) Preparation of starane residues determination in soil, water and wheat. Agrochemicals 48:120–122Google Scholar
  41. Torres MA, Barros MP, Campos SCG, Pinto E, Rajamani S, Sayre RT, Colepicolo P (2008) Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol Environ Saf 71:1–15CrossRefGoogle Scholar
  42. United States Environmental Protection Agency (1998). Pesticide fact sheet, name of chemical: fluroxypyr, reason for issuance: conditional registration date issued: September 30Google Scholar
  43. Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390CrossRefGoogle Scholar
  44. Vartak V, Bhargava S (1999) Photosynthetic performance and antioxidant metabolism in a paraquat-resistant mutant of Chlamydomonas reinhardtii L. Pestic Biochem Physiol 64:9–15CrossRefGoogle Scholar
  45. Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923CrossRefGoogle Scholar
  46. Wang SH, Yang ZM, Lu B, Li SQ, Lu YP (2004) Copper-induced stress and antioxidative responses in roots of Brassica juncea L. Bot Bull Acade Sin 45:203–212Google Scholar
  47. Wang XD, Liu XJ, Yang S, Li AL, Yang YL (2007) Removal and toxicological response of triazophos by Chlamydomonas reinhardtii. Bull Environ Contam Toxicol 78:67–71CrossRefGoogle Scholar
  48. Woodbury W, Spencer AK, Stahmann MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305CrossRefGoogle Scholar
  49. Wu GL, Cui J, Tao L, Yang H (2010) Fluroxypyr triggers oxidative damage by producing superoxide and hydrogen peroxide in rice (Oryza sativa). Ecotoxicology 19:124–132CrossRefGoogle Scholar
  50. Yin XL, Jiang L, Song NH, Yang H (2008) Toxic reactivity of wheat (Triticum aestivum) plants to herbicide isoproturon. J Agric Food Chem 56:4825–4831CrossRefGoogle Scholar
  51. Yoshida K, Igarashi E, Wakatsuki E, Miyamoto K, Hirata K (2004) Mitigation of osmotic and salt stresses by abscisic acid through reduction of stress-derived oxidative damage in Chlamydomonas reinhardtii. Plant Sci 167:1335–1341CrossRefGoogle Scholar
  52. Yu LQ, Yoshiharu F, Zhou YJ, Zhang JP, Lu YL (2007) Response of exotic invasive weed Alternanthera philoxeroides to environmental factors and its competition with rice. Rice Sci 14:49–55CrossRefGoogle Scholar
  53. Zhang LP, Mehta SK, Liu ZP, Yang ZM (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Shuang Zhang
    • 1
    • 3
  • Chong Bin Qiu
    • 1
    • 3
  • You Zhou
    • 1
    • 3
  • Zhen Peng Jin
    • 1
    • 2
    • 3
  • Hong Yang
    • 1
    • 2
    • 3
  1. 1.Department of Applied Chemistry, College of ScienceNanjing Agricultural UniversityNanjingChina
  2. 2.Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects of Ministry of Agriculture, College of ScienceNanjingChina
  3. 3.Jiangsu Key Laboratory of Pesticide Science, Nanjing Agricultural University, College of ScienceNanjingChina

Personalised recommendations