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

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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.

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References

  • APHA (1998) Methods for biomass production. In: Standard methods for the examination of water and wastewater. American Public Health Association, Baltimore MD

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 1–95

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cherry JH, Nielsen BL (2004) Metabolic engineering of chloroplasts for abiotic stress tolerance. In: Molecular biology and biotechnology of plant organelles, pp 513–525

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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–B23

    Google Scholar 

  • 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 106:97–109

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 62:2773–2777

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lepage G, Roy CC (1984) Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396

    CAS  Google Scholar 

  • 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 28:1534–1538

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 

  • Motulsky HJ (2007) Prism 5 statistics guide. GraphPad Software Inc., San Diego CA

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pinto G, Pollio A, Previtera L, Temussi F (2002) Biodegradation of phenols by microalgae. Biotechnol Lett 24:2047–2051. doi:10.1023/A:1021367304315

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 6:648–653

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • US Environmental Protection Agency (2002) Short-term methods for estimating chronic toxicity of effluents and receiving water to freshwater organisms, 4th edn. Washington DC

  • US Environmental Protection Agency (2012) Atrazine updates. Washington DC

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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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.

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Kabra, A.N., Ji, MK., Choi, J. et al. Toxicity of atrazine and its bioaccumulation and biodegradation in a green microalga, Chlamydomonas mexicana . Environ Sci Pollut Res 21, 12270–12278 (2014). https://doi.org/10.1007/s11356-014-3157-4

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