Advertisement

Environmental Science and Pollution Research

, Volume 21, Issue 21, pp 12270–12278 | Cite as

Toxicity of atrazine and its bioaccumulation and biodegradation in a green microalga, Chlamydomonas mexicana

  • Akhil N. Kabra
  • Min-Kyu Ji
  • Jaewon Choi
  • Jung Rae Kim
  • Sanjay P. Govindwar
  • Byong-Hun Jeon
Research Article

Abstract

This study evaluated the toxicity of herbicide atrazine, along with its bioaccumulation and biodegradation in the green microalga Chlamydomonas mexicana. At low concentration (10 μg L−1), atrazine had no profound effect on the microalga, while higher concentrations (25, 50, and 100 μg L−1) imposed toxicity, leading to inhibition of cell growth and chlorophyll a accumulation by 22 %, 33 %, and 36 %, and 13 %, 24 %, and 27 %, respectively. Atrazine 96-h EC50 for C. mexicana was estimated to be 33 μg L−1. Microalga showed a capability to accumulate atrazine in the cell and to biodegrade the cell-accumulated atrazine resulting in 14–36 % atrazine degradation at 10–100 μg L−1. Increasing atrazine concentration decreased the total fatty acids (from 102 to 75 mg g−1) and increased the unsaturated fatty acid content in the microalga. Carbohydrate content increased gradually with the increase in atrazine concentration up to 15 %. This study shows that C. mexicana has the capability to degrade atrazine and can be employed for the remediation of atrazine-contaminated streams.

Keywords

Atrazine Chlamydomonas mexicana Bioaccumulation Biodegradation Fatty acid Carbohydrate 

Notes

Acknowledgments

This work was supported by the Yonsei University Research Fund of 2013, the Mid-career Researcher Program [National Research Foundation of Korea (NRF) grant, 2013069183], the Small & Medium Business Administration (SMBA) grant C0103527 through the Academic-Industrial Common Technology Development Project, and the Eco-Innovation Project (Global-Top Project) of the Korea Ministry of Environment.

References

  1. APHA (1998) Methods for biomass production. In: Standard methods for the examination of water and wastewater. American Public Health Association, Baltimore MDGoogle Scholar
  2. Baun A, Sorensen SN, Rasmussen RF, Hartmann NB, Koch CB (2008) Toxicity and bioaccumulation of xenobiotic organic compounds in the presence of aqueous suspensions of aggregates of nano-C60. Aquat Toxicol 86:379–387. doi: 10.1016/j.aquatox.2007.11.019 CrossRefGoogle Scholar
  3. Bi YF, Miao SS, Lu YC, Qiu CB, Zhou Y, Yang H (2012) Phytotoxicity, bioaccumulation and degradation of isoproturon in green algae. J Hazard Mater 243:242–249. doi: 10.1016/j.jhazmat.2012.10.021 CrossRefGoogle Scholar
  4. Bischoff HW, Bold HC (1963) Phycological Studies IV. In: Some soil algae from enchanted rock and related algal species. University of Texas Publication, Austin, pp 1–95Google Scholar
  5. Bodalo A, Leon G, Hidalgo AM, Gomez M, Murcia MD, Blanco P (2010) Atrazine removal from aqueous solutions by nanofiltration. Desalin Wat Treat 3:143–148. doi: 10.5004/dwt.2010.986 CrossRefGoogle Scholar
  6. Branyikova I, Marsalkova B, Doucha J, Branyik T, Bisova K, Zachleder V, Vítova M (2011) Microalgae-novel highly efficient starch producers. Biotechnol Bioeng 108:766–776. doi: 10.1002/bit.23016 CrossRefGoogle Scholar
  7. Carrieri D, Momot D, Brasg IA, Ananyev G, Lenz O, Bryant DA, Dismukes GC (2010) Boosting auto fermentation rates and product yields with sodium stress cycling: application to production of renewable fuels by cyanobacteria. Appl Environ Microbiol 76:6455–6462. doi: 10.1128/AEM.00975-10 CrossRefGoogle Scholar
  8. Cherry JH, Nielsen BL (2004) Metabolic engineering of chloroplasts for abiotic stress tolerance. In: Molecular biology and biotechnology of plant organelles, pp 513–525Google Scholar
  9. Collings AF, Gwan PB (2010) Ultrasonic destruction of pesticide contaminants in slurries. Ultrason Sonochem 17:1–3. doi: 10.1016/j.ultsonch.2009.05.001 CrossRefGoogle Scholar
  10. de Morais MG, Costa JAV (2007) Biofixation of carbon dioxide by Spirulina sp. and Scenedesmus obliquus cultivated in a three stage serial tubular photobioreactor. J Biotechnol 129:439–445. doi: 10.1016/j.jbiotec.2007.01.009 CrossRefGoogle Scholar
  11. Debelius B, Forja JM, Valls AD, Lubian LM (2008) Effect of linear alkylbenzene sulfonate (LAS) and atrazine on marine microalgae. Mar Pollut Bull 57:559–568. doi: 10.1016/j.marpolbul.2008.01.040 CrossRefGoogle Scholar
  12. Dombek T, Dolan E, Schultz J, Klarup D (2001) Rapid reductive dechlorination of atrazine by zero-valent iron under acidic conditions. Environ Pollut 111:21–27. doi: 10.1016/S0269-7491(00)00033-6 CrossRefGoogle Scholar
  13. El-Salam Issa A, Adam MS, Fawzy MA (2013) Alterations in some metabolic activities of Scenedesmus quadricauda and Merismopedia glauca in response to glyphosate herbicide. J Biol Earth Sci 3:B17–B23Google Scholar
  14. Fournadzhieva S, Kassabov P, Andreeva R, Petkov G, Dittrit F (1995) Influence of the herbicide simazine on Chlorella, Scenedesmus and Arthrospira. Int J Phycological Res 106:97–109Google Scholar
  15. Gonzalez-Barreiro O, Rioboo C, Herrero C, Cid A (2006) Removal of triazine herbicides from freshwater systems using photosynthetic microorganisms. Environ Pollut 144:266–271. doi: 10.1016/j.envpol.2005.12.014 CrossRefGoogle Scholar
  16. Graymore M, Stagnitti F, Allinson G (2001) Impacts of atrazine on aquatic ecosystems. Environ Int 26:483–495. doi: 10.1016/S0160-4120(01)00031-9 CrossRefGoogle Scholar
  17. Hayes TB, Khoury V, Narayan A, Nazir M, Park A, Brown T, Adame L, Chan E, Buchholz D, Stueve T, Gallipeau S (2010) Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). PNAS 107:4612–4617. doi: 10.1073/pnas.0909519107 CrossRefGoogle Scholar
  18. Heipieper HJ, Meulenbeld G, Oirschot QV, de Bont J (1996) Effect of environmental factors on the trans/cis ratio of unsaturated fatty acids in Pseudomonas putida S12. Appl Environ Microbiol 62:2773–2777Google Scholar
  19. Hirooka T, Nagase H, Uchida K, Hiroshige Y, Ehara Y, Nishikawa J, Nishihara T, Miyamoto K, Hirata Z (2005) Biodegradation of bisphenol A and disappearance of its estrogenic activity by the green alga Chlorella fusca var. vacuolata. Environ Toxicol Chem 24:1896–1901. doi: 10.1897/04-259R.1 CrossRefGoogle Scholar
  20. Ji MK, Kim HC, Sapireddy VR, Yun HS, Abou-Shanab RAI, Choi J, Lee W, Timmes TC, Inamuddin JBH (2013a) Simultaneous nutrient removal and lipid production from pretreated piggery wastewater by Chlorella vulgaris YSW-04. Appl Microbiol Biotechnol 97:2701–2710. doi: 10.1007/s00253-012-4097-x CrossRefGoogle Scholar
  21. Ji MK, Abou-Shanab RAI, Kim SH, Salama E-S, Lee SH, Kabra AN, Lee YS, Hong S, Jeon BH (2013b) Cultivation of microalgae species in tertiary municipal wastewater supplemented with CO2 for nutrient removal and biomass production. Ecol Eng 58:142–148. doi: 10.1016/j.ecoleng.2013.06.020 CrossRefGoogle Scholar
  22. Jin ZP, Luo K, Zhang S, Zheng Q, Yang H (2012) Bioaccumulation and catabolism of prometryne in green algae. Chemosphere 87:278–284. doi: 10.1016/j.chemosphere.2011.12.071 CrossRefGoogle Scholar
  23. Juneja A, Ceballos RM, Murthy GS (2013) Effects of environmental factors and nutrient availability on the biochemical composition of algae for biofuels production: a review. Energies 6:4607–4638. doi: 10.3390/en6094607 CrossRefGoogle Scholar
  24. Kolekar PD, Phugare SS, Jadhav JP (2014) Biodegradation of atrazine by Rhodococcus sp. BCH2 to N-isopropylammelide with subsequent assessment of toxicity of biodegraded metabolites. Environ Sci Pollut Res 21:2334–2345. doi: 10.1007/s11356-013-2151-6 CrossRefGoogle Scholar
  25. Kumar MS, Praveenkumar R, Ilavarasi A, Rajeshwari K, Thajuddin N (2012) Oxidative stress response and fatty acid changes associated with bioaccumulation of chromium [Cr(VI)] by a freshwater cyanobacterium Chroococcus sp. Biotechnol Lett 34:247–251. doi: 10.1007/s10529-011-0771-9 CrossRefGoogle Scholar
  26. Lackhoff M, Niessner R (2002) Photocatalytic atrazine degradation by synthetic minerals, Atmospheric Aerosols, and Soil Particles. Environ Sci Technol 36:5342–5347. doi: 10.1021/es025590a CrossRefGoogle Scholar
  27. Lepage G, Roy CC (1984) Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396Google Scholar
  28. Li FM, Hu HY, Chong YX, Men YJ, Guo MT (2007) Effects of allelochemical EMA isolated from Phragmites communis on algal cell membrane lipid and ultrastructure. Chinese J Environ Sci 28:1534–1538Google Scholar
  29. Li R, Chen GZ, Tam NF, Luan TG, Shin PK (2009) Toxicity of bisphenol A and its bioaccumulation and removal by a marine microalga Stephanodiscus hantzschii. Ecotoxicol Environ Saf 72:321–328. doi: 10.1016/j.ecoenv.2008.05.012 CrossRefGoogle Scholar
  30. Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049. doi: 10.1007/s10529-009-9975-7 CrossRefGoogle Scholar
  31. Lieu SN, Kerhoas L, Einhorn J (2000) Degradation of atrazine into ammeline by combined ozone/hydrogen peroxide treatment in water. Environ Sci Technol 34:430–437. doi: 10.1021/es980540k CrossRefGoogle Scholar
  32. Liu Y, Luan TG, Lu NN, Lan CY (2006) Toxicity of fluoranthene and its biodegradation by Cyclotella caspia Alga. J Integrative Plant Biol 48:169–180. doi: 10.1111/j.1744-7909.2006.00161.x-i1 CrossRefGoogle Scholar
  33. Liu X, Li WJ, Li L, Yang Y, Mao LG, Penga Z (2014) A label-free electrochemical immunosensor based on gold nanoparticles for direct detection of atrazine. Sensors and Actuators B 191:408–414. doi: 10.1016/j.snb.2013.10.033 CrossRefGoogle Scholar
  34. Marchetti G, Minella M, Maurino V, Minero C, Vione D (2013) Photochemical transformation of atrazine and formation of photointermediates under conditions relevant to sunlit surface waters: laboratory measures and modeling. Wat Res 47:6211–6222. doi: 10.1016/j.watres.2013.07.038 CrossRefGoogle Scholar
  35. Mattoo AK, St. John JB, Wergin WP (1984) Adaptive reorganization of protein and lipid components in chloroplast membranes as associated with herbicide binding. J Cell Biochem 24:145–163. doi: 10.1002/jcb.240240207 CrossRefGoogle Scholar
  36. Mayasich JM, Karlander EP, Terlizzi DE (1986) Growth responses of Nannochloris oculata Droop and Phaeodactylum tricornutum Bohlin to the herbicide atrazine as influenced by light intensity and temperature. Aquat Toxicol 8:175–184. doi: 10.1016/0166-445X(87)90011-7 CrossRefGoogle Scholar
  37. Mofeed J, Mosleha YY (2013) Toxic responses and antioxidative enzymes activity of Scenedesmus obliquus exposed to fenhexamid and atrazine, alone and in mixture. Ecotoxicol Environ Saf 95:234–240. doi: 10.1016/j.ecoenv.2013.05.023 CrossRefGoogle Scholar
  38. Mostafa M, Kotkat HM, Hammouda OH (1994) Effect of atrazine herbicide on growth, photosynthesis, protein synthesis, and fatty acid composition in the unicellular green alga Chlorella kessleri. Ecotoxicol Environ Saf 29:349–358. doi: 10.1016/0147-6513(94)90007-8 CrossRefGoogle Scholar
  39. Mostafa M, Ghareib MM, Abou-EL-Souod GW (2011) Biodegradation of phenolic and polycyclic aromatic compounds by some algae and cyanobacteria. J Bioremed Biodeg 3:1–9. doi: 10.1016/0147-6513(94)90007-8 Google Scholar
  40. Motulsky HJ (2007) Prism 5 statistics guide. GraphPad Software Inc., San Diego CAGoogle Scholar
  41. Nwachukwu EO, Osuji JO (2007) Bioremedial degradation of some herbicides by indigenous white rot fungus, Lentinus subnudus. J Plant Sci 2:619–624. doi: 10.3923/jps.2007.619.624 CrossRefGoogle Scholar
  42. Pinto G, Pollio A, Previtera L, Temussi F (2002) Biodegradation of phenols by microalgae. Biotechnol Lett 24:2047–2051. doi: 10.1023/A:1021367304315 CrossRefGoogle Scholar
  43. Porra RJ, Thompson WA, Kriedmann PE (1989) Determination of accurate extinction co-efficients 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. Biochem Biophys Acta 975:384–394. doi: 10.1016/S0005-2728(89)80347-0 Google Scholar
  44. Ramel F, Sulmon C, Bogard M, Couee I, Gouesbet G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol 9:28. doi: 10.1186/1471-2229-9-28 CrossRefGoogle Scholar
  45. Rao P, Pattabiraman TN (1989) Reevaluation of the phenol–sulfuric acid reaction for the estimation of hexoses and pentoses. Anal Biochem 181:18–22. doi: 10.1016/0003-2697(89)90387-4 CrossRefGoogle Scholar
  46. Rashid U, Anwar F, Moser BR, Knothe G (2008) Moringa oleifera oil: a possible source of biodiesel. Bioresour Technol 99:8175–8179. doi: 10.1016/j.biortech.2008.03.066 CrossRefGoogle Scholar
  47. Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 6:648–653CrossRefGoogle Scholar
  48. Schroder P, Harvey PJ, Schwitzguebel JP (2002) Prospects for the phytoremediation of organic pollutants in Europe. Environ Sci Pollut Res 9:1–3. doi: 10.1007/BF02987312 CrossRefGoogle Scholar
  49. Semple KT, Cain RB, Schmidt S (1999) Biodegradation of aromatic compounds by microalgae. FEMS Microbiol Lett 170:291–300. doi: 10.1016/S0378-1097(98)00544-8 CrossRefGoogle Scholar
  50. Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R (2013) Mixotrophic cyanobacteria and microalgae as distinctive biological agents for organic pollutant degradation. Environ Int 5:59–72. doi: 10.1016/j.envint.2012.10.007 CrossRefGoogle Scholar
  51. Tang J, Hoagland KD, Siegfried BD (1998)) Uptake and bioconcentration of atrazine by selected freshwater algae. Environ Toxicol Chem 17:1085–1090. doi: 10.1897/1551-5028(1998)017<1085:UABOAB>2.3.CO;2 CrossRefGoogle Scholar
  52. Torres AMR, O’Flaherty LM (1976) Influence of pesticides on Chlorella, Chlorococcum, Stigeoclonium (Chlorophyceae), Tribonema, Vaucheria (Xanthophyccae) and Oscillatoria (Cyanophyceae). Phycologia 15:25–36. doi: 10.2216/i0031-8884-15-1-25.1 CrossRefGoogle Scholar
  53. US Environmental Protection Agency (2002) Short-term methods for estimating chronic toxicity of effluents and receiving water to freshwater organisms, 4th edn. Washington DCGoogle Scholar
  54. US Environmental Protection Agency (2012) Atrazine updates. Washington DCGoogle Scholar
  55. Vonberg D, Vanderborght J, Cremer N, Putz T, Herbst M, Vereecken H (2013) 20 years of long-term atrazine monitoring in a shallow aquifer in western Germany. Wat Res 50:294–306. doi: 10.1016/j.watres.2013.10.032 CrossRefGoogle Scholar
  56. Weiner AJ, Delorenzo ME, Fulton MH (2004) Relationship between uptake capacity and differential toxicity of the herbicide atrazine in selected microalgal species. Aquat Toxicol 68:121–128. doi: 10.1016/j.aquatox.2004.03.004 CrossRefGoogle Scholar
  57. Zhang S, Qiu CB, Zhou Y, Jin ZP, Yang H (2011) Bioaccumulation and degradation of pesticide fluroxypyr are associated with toxic tolerance in green alga Chlamydomonas reinhardtii. Ecotoxicol 20:337–347. doi: 10.1007/s10646-010-0583-z CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Akhil N. Kabra
    • 1
  • Min-Kyu Ji
    • 1
  • Jaewon Choi
    • 2
  • Jung Rae Kim
    • 3
  • Sanjay P. Govindwar
    • 4
  • Byong-Hun Jeon
    • 1
  1. 1.Department of Environmental EngineeringYonsei UniversityWonjuSouth Korea
  2. 2.Water Analysis and Research Center, Korea Institute of Water and EnvironmentKorea Water Resources Corp.DaejeonSouth Korea
  3. 3.School of Chemical and Biomolecular EngineeringPusan National UniversityBusanSouth Korea
  4. 4.Department of BiochemistryShivaji UniversityKolhapurIndia

Personalised recommendations