Advertisement

Sensitivity of selected tropical microalgae isolated from a farmland and a eutrophic lake to atrazine and endosulfan

  • Yin-Yien Chin
  • Wan-Loy ChuEmail author
  • Yih-Yih Kok
  • Siew-Moi Phang
  • Chiew-Yen Wong
  • Boon-Keat Tan
  • Emienour Muzalina Mustafa
Article

Abstract

There has been concern over the adverse ecotoxicological effects of atrazine and endosulfan on microalgae. This study aimed to assess the effects of these two widely used pesticides on growth, pigmentation, and oxidative response of microalgal isolates from a farmland and a eutrophic lake in Malaysia, in comparison with the model species Pseudokirchneriella subcapitata. Results showed that the microalgae originated from the eutrophic lake were generally more sensitive to the pesticides than those from the farmland. The microalgae were more sensitive to atrazine (EC50 = 43.07–> 5000 μg L−1) than endosulfan (EC50 = 1.51–> 50 mg L−1). Amongst the microalgae, Scenedesmus arcuatus was most sensitive to atrazine (EC50 = 43.07 μg L−1) while Chlorella sp. 1 was most sensitive to endosulfan (EC50 = 1.51 mg L−1). Microalgae from the farmland were generally very tolerant to endosulfan (EC50 > 50 mg L−1). Photosynthetic pigment content (pg cell−1) increased in S. arcuatus after exposure to atrazine while the content decreased in most of the microalgae after exposure to endosulfan. Oxidative response to the pesticides varied amongst the tested microalgae and time point measured. Both ROS levels and lipid peroxidation decreased in Chlorella sp. 5 after exposure to atrazine at 96 h compared to 48 h. In S. arcuatus, there was no pronounced increase in SOD and catalase activities despite the increase in ROS and lipid peroxidation after exposure to atrazine. Indigenous microalgae such as S. arcuatus could be a useful bioassay organism for toxicity testing of the pesticides while tolerant species from the farmland could be useful for bioremediation of endosulfan contamination.

Keywords

Atrazine Endosulfan Microalgae Oxidative stress Chlorella Scenedesmus 

Notes

Acknowledgments

The first author would like to express her appreciation to MOE for the MyBrain Scholarship in supporting her doctoral study.

Funding information

This research project received funding support from the Fundamental Research Grant Scheme (FRGS) from the Ministry of Education (MOE), Malaysia (FRGS/2/2014/STWN01/IMU/01/1).

Supplementary material

10811_2019_1800_MOESM1_ESM.docx (5.2 mb)
ESM 1 (DOCX 5310 kb)

References

  1. Abdullah PM, Abdul Aziz YF, Rozali Othman M, Wan Mohd Khalik WMA (2015) Organochlorine pesticides residue level in surface water of Cameron Highlands, Malaysia. Iranica J Energy Environ 6Google Scholar
  2. Ahmad AL, Tan LS, Shukor SR (2008) Dimethoate and atrazine retention from aqueous solution by nanofiltration membranes. J Hazard Mater 151:71–77CrossRefGoogle Scholar
  3. Anonymous (2017) NIES collection - microbial culture collection - strain data. http://mcc.nies.go.jp/strainList.do?strainId=26&strainNumberEn=NIES-35. Accessed 9 June 2018
  4. Bai X, Sun C, Xie J, Song H, Zhu Q, Su Y, Qian H, Fu Z (2015) Effects of atrazine on photosynthesis and defense response and the underlying mechanisms in Phaeodactylum tricornutum. Environ Sci Pollut Res Int 22:17499–17507CrossRefGoogle Scholar
  5. Baxter L, Brain RA, Lissemore L, Solomon KR, Hanson ML, Prosser RS (2016) Influence of light, nutrients, and temperature on the toxicity of atrazine to the algal species Raphidocelis subcapitata: implications for the risk assessment of herbicides. Ecotoxicol Environ Saf 132:250–259CrossRefGoogle Scholar
  6. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefGoogle Scholar
  7. Behra R, Genoni G, Joseph A (1999) Effect of atrazine on growth, photosynthesis, and between-strain variability in Scenedesmus subspicatus (Chlorophyceae). Arch Environ Contam Toxicol 37:36–41CrossRefGoogle Scholar
  8. Berard A, Leboulanger C, Pelte T (1999) Tolerance of Oscillatoria limnetica Lemmermann to atrazine in natural phytoplankton populations and in pure culture: influence of season and temperature. Arch Environ Contam Toxicol 37:472–479CrossRefGoogle Scholar
  9. Berard A, Rimet F, Capowiez Y, Leboulanger C (2004) Procedures for determining the pesticide sensitivity of indigenous soil algae: a possible bioindicator of soil contamination? Arch Environ Contam Toxicol 46:24–31CrossRefGoogle Scholar
  10. Blaise C, Vasseur P (2005) Algal microplate toxicity test. In: Blaise C, Férard JF (eds) Small-scale freshwater toxicity investigations. Springer, Dordrecht, pp 137–179CrossRefGoogle Scholar
  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  12. Camuel A, Guieysse B, Alcantara C, Bechet Q (2017) Fast algal eco-toxicity assessment: influence of light intensity and exposure time on Chlorella vulgaris inhibition by atrazine and DCMU. Ecotoxicol Environ Saf 140:141–147CrossRefGoogle Scholar
  13. CAP (Consumers Association of Penang) 2010. Is our rice safe from banned endosulfan? http://consumer.org.my/food/safety/140-is-our-rice-safe-from-banned-endosulfan. Accessed 5 October 2018
  14. Cheloni G, Slaveykova VI (2013) Optimization of the C11-BODIPY581/591 dye for the determination of lipid oxidation in Chlamydomonas reinhardtii by flow cytometry. Cytometry 83:952–961Google Scholar
  15. Chia MA, Dauda S, Jibril TZ (2016) Toxicity of atrazine to Scenedesmus quadricauda under different nitrogen concentrations. Environ Earth Sci 75:960CrossRefGoogle Scholar
  16. Daam MA, van den Brink PJ (2010) Implications of differences between temperate and tropical freshwater ecosystems for the ecological risk assessment of pesticides. Ecotoxicology 19:24–37CrossRefGoogle Scholar
  17. Davis AM, Lewis SE, Bainbridge ZT, Glendenning L, Turner RD, Brodie JE (2012) Dynamics of herbicide transport and partitioning under event flow conditions in the lower Burdekin region, Australia. Mar Pollut Bull 65:182–193CrossRefGoogle Scholar
  18. DeLorenzo ELA, Taylor SALM (2002) Toxicity and bioconcentration potential of the agricultural pesticide endosulfan in phytoplankton and zooplankton. Arch Environ Contam Toxicol 42:173–181CrossRefGoogle Scholar
  19. DeLorenzo ME, Leatherbury M, Weiner JA, Lewitus AJ, Fulton MH (2004) Physiological factors contributing to the species-specific sensitivity of four estuarine microalgal species exposed to the herbicide atrazine. Aquat Ecosyst Health Manage 7:137–146CrossRefGoogle Scholar
  20. Downie D (2003) Global POPs policy: the 2001 Stockholm convention on persistent organic pollutants. In: Downie D, Fenge T (eds) Northern lights against POPs: combating toxic threats in the Arctic. McGill-Queens University Press, Montreal, pp 133–159Google Scholar
  21. Duke SO (1990) Overview of herbicide mechanisms of action. Environ Health Perspect 87:263–271CrossRefGoogle Scholar
  22. Esperanza M, Houde M, Seoane M, Cid A, Rioboo C (2017) Does a short-term exposure to atrazine provoke cellular senescence in Chlamydomonas reinhardtii? Aquat Toxicol 189:184–193CrossRefGoogle Scholar
  23. Fairchild JF, Ruessler DS, Carlson AR (1998) Comparative sensitivity of five species of macrophytes and six species of algae to atrazine, metribuzin, alachlor, and metolachlor. Environ Toxicol Chem 17:1830–1834CrossRefGoogle Scholar
  24. FAO (Food and Agricultural Organisation) (2016) Prevention and disposal of obsolete pesticides. http://www.fao.org/agriculture/crops/obsolete-pesticides/prevention-and-disposal-of-obsolete-pesticides/en/. Accessed 5 October 2018
  25. Fernández-Naveira A, Rioboo C, Cid A, Herrero C (2016) Atrazine induced changes in elemental and biochemical composition and nitrate reductase activity in Chlamydomonas reinhardtii. Eur J Phycol 51:338–345CrossRefGoogle Scholar
  26. Flood SL, Burkholder JM (2018) Chattonella subsalsa (Raphidophyceae) growth and hemolytic activity in response to agriculturally-derived estuarine contaminants. Harmful Algae 76:66–79CrossRefGoogle Scholar
  27. González-Barreiro Ó, Rioboo C, Cid A, Herrero C (2004) Atrazine-induced chlorosis in Synechococcus elongatus cells. Arch Environ Contam Toxicol 46:301–307CrossRefGoogle Scholar
  28. Graymore M, Stagnitti F, Allinson G (2001) Impacts of atrazine in aquatic ecosystems. Environ Int 26:483–495CrossRefGoogle Scholar
  29. Guo R, Lee MA, Ki JS (2013) Different transcriptional responses of heat shock protein 70/90 in the marine diatom Ditylum brightwellii exposed to metal compounds and endocrine-disrupting chemicals. Chemosphere 92:535–543CrossRefGoogle Scholar
  30. Helweg A, Bay H, Hansen HPB, Rabølle M, Sonnenborg A, Stenvang L (2002) Pollution at and below sites used for mixing and loading of pesticides. Int J Environ Anal Chem 82:583–590CrossRefGoogle Scholar
  31. Hii YS, Shia KL, Chuah TS, Hing LS (2009) Physiological responses of Chaetoceros sp. and Nannochloropsis sp. to short-term 2, 4-D, dimethylamine and endosulfan exposure. Aquat Ecosyst Health Manage 12:375–389CrossRefGoogle Scholar
  32. Hogue C (2011) Endosulfan banned worldwide. Chem Eng News 89(19):15Google Scholar
  33. Howe PL, Reichelt-Brushett AJ, Clark MW, Seery CR (2017) Toxicity estimates for diuron and atrazine for the tropical marine cnidarian Exaiptasia pallida and in-hospite Symbiodinium spp. using PAM chlorophyll-a fluorometry. J Photochem Photobiol B 171:125–132CrossRefGoogle Scholar
  34. Jablonowski ND, Schäffer A, Burauel P (2011) Still present after all these years: persistence plus potential toxicity raise questions about the use of atrazine. Environ Sci Pollut Res Int 18:328–331CrossRefGoogle Scholar
  35. Kegley SE, Hill BR, Orme S, Choi AH (2010) PAN pesticide database. Pesticide Action Network, North America http:www.pesticideinfo.org. Accessed 7 October 2018Google Scholar
  36. Kumar S, Habib K, Fatma T (2008) Endosulfan induced biochemical changes in nitrogen-fixing cyanobacteria. Sci Total Environ 403:130–138CrossRefGoogle Scholar
  37. Kumar N, Bora A, Kumar R, Amb MK (2012) Differential effects of agricultural pesticides endosulfan and tebuconazole on photosynthetic pigments, metabolism and assimilating enzymes of three heterotrophic, filamentous cyanobacteria. J Biol Environ Sci 6:67–75Google Scholar
  38. Kwon CS, Penner D (1995) The interaction of insecticides with herbicide activity. Weed Technol 9:119–124CrossRefGoogle Scholar
  39. Li Y, Schellhorn HE (2007) Rapid kinetic microassay for catalase activity. J Biomol Tech 18:185–187Google Scholar
  40. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protocol Food Anal Chem F4:1 (Supplement 1)Google Scholar
  41. Ma J, Lin F, Wang S, Xu L (2003) Toxicity of 21 herbicides to the green alga Scenedesmus quadricauda. Bull Environ Contam Toxicol 71:594–601CrossRefGoogle Scholar
  42. Magnusson M, Heimann K, Negri AP (2008) Comparative effects of herbicides on photosynthesis and growth of tropical estuarine microalgae. Mar Pollut Bull 56:1545–1552CrossRefGoogle Scholar
  43. Majewska M, Harshkova D, Gusciora M, Aksmann A (2018) Phytotoxic activity of diclofenac: evaluation using a model green alga Chlamydomonas reinhardtii with atrazine as a reference substance. Chemosphere 209:989–997CrossRefGoogle Scholar
  44. Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193CrossRefGoogle Scholar
  45. Menezes RG, Qadir TF, Moin A, Fatima H, Hussain SA, Madadin M, Pasha SB, Al Rubaish FA, Senthilkumaran S (2017) Endosulfan poisoning: an overview. J Forensic Legal Med 51:27–33CrossRefGoogle Scholar
  46. Mohapatra P, Mohanty R (1992) Growth pattern changes of Chlorella vulgaris and Anabaena doliolum due to toxicity of dimethoate and endosulfan. Bull Environ Contam Toxicol 49:576–581CrossRefGoogle Scholar
  47. Nichols HW (1973) Growth media - freshwater. In: Stein JR (ed) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, Cambridge, pp 7–24Google Scholar
  48. Noctor G, Lelarge-Trouverie C, Mhamdi A (2015) The metabolomics of oxidative stress. Phytochemistry 112:33–53CrossRefGoogle Scholar
  49. Norberg-King T (1993) A linear interpolation method for sublethal toxicity: the inhibition concentration (ICp) approach. National Effluent Toxicity Assessment Center Technical Report, Version 2, vol 2, pp 3–93Google Scholar
  50. OECD (Organisation for Economic Co-operation and Development) (2011) Test no. 201: freshwater alga and cyanobacteria, growth inhibition test, OECD guidelines for the testing of chemicals, Section 2. OECD Publishing, Paris, p 25Google Scholar
  51. Ogawa Y, Kobayashi T, Nishioka A, Kariya S, Hamasato S, Seguchi H, Yoshida S (2003) Radiation-induced reactive oxygen species formation prior to oxidative DNA damage in human peripheral T cells. Int J Mol Med 11:149–152Google Scholar
  52. Petersen K, Heiaas HH, Tollefsen KE (2014) Combined effects of pharmaceuticals, personal care products, biocides and organic contaminants on the growth of Skeletonema pseudocostatum. Aquat Toxicol 150:45–54CrossRefGoogle Scholar
  53. Prasad SM, Kumar D, Zeeshan M (2005) Growth, photosynthesis, active oxygen species and antioxidants responses of paddy field cyanobacterium Plectonema boryanum to endosulfan stress. J Gen Appl Microbiol 51:115–123CrossRefGoogle Scholar
  54. Prasad SM, Zeeshan M, Kumar D (2011) Toxicity of endosulfan on growth, photosynthesis, and nitrogenase activity in two species of Nostoc (Nostoc muscorum and Nostoc calcicola). Toxicol Environ Chem 93:513–525CrossRefGoogle Scholar
  55. Qian H, Daniel Sheng G, Liu W, Lu Y, Liu Z, Fu Z (2008) Inhibitory effects of atrazine on Chlorella vulgaris as assessed by real-time polymerase chain reaction. Environ Toxicol Chem 27:182–187CrossRefGoogle Scholar
  56. Ricart M, Barcelo D, Geiszinger A, Guasch H, de Alda ML, Romani AM, Vidal G, Villagrasa M, Sabater S (2009) Effects of low concentrations of the phenylurea herbicide diuron on biofilm algae and bacteria. Chemosphere 76:1392–1401CrossRefGoogle Scholar
  57. Roger PA, Ladha JK (1992) Biological N2 fixation in wetland rice fields: estimation and contribution to nitrogen balance. Plant Soil 141:41–55CrossRefGoogle Scholar
  58. Saadati N, Abdullah MP, Zakaria Z, Rezayi M, Hosseinizare N (2012) Distribution and fate of HCH isomers and DDT metabolites in a tropical environment–case study Cameron Highlands–Malaysia. Chem Central J 6:130–130CrossRefGoogle Scholar
  59. Sass JB, Colangelo A (2006) European Union bans atrazine, while the United States negotiates continued use. Int J Occup Environ Health 12:260–267CrossRefGoogle Scholar
  60. Seguin F, Le Bihan F, Leboulanger C, Bérard A (2002) A risk assessment of pollution: induction of atrazine tolerance in phytoplankton communities in freshwater outdoor mesocosms, using chlorophyll fluorescence as an endpoint. Water Res 36:3227–3236CrossRefGoogle Scholar
  61. Sethunathan N, Megharaj M, Chen ZL, Williams BD, Lewis G, Naidu R (2004) Algal degradation of a known endocrine disrupting insecticide, α-endosulfan, and its metabolite, endosulfan sulfate, in liquid medium and soil. J Agric Food Chem 52:3030–3035CrossRefGoogle Scholar
  62. Silva MH, Beauvais SL (2010) Human health risk assessment of endosulfan. I: toxicology and hazard identification. Regul Toxicol Pharmacol 56:4–17CrossRefGoogle Scholar
  63. Tang JX, Hoagland KD, Siegfried BD (1997) Differential toxicity of atrazine to selected freshwater algae. Bull Environ Contam Toxicol 59:631–637CrossRefGoogle Scholar
  64. Tang J, Hoagland KD, Siegfried BD (1998) Uptake and bioconcentration of atrazine by selected freshwater algae. Environ Toxicol Chem 17:1085–1090CrossRefGoogle Scholar
  65. Tasmin R, Shimasaki Y, Tsuyama M, Qiu X, Khalil F, Okino N, Yamada N, Fukuda S, Kang IJ, Oshima Y (2014) Elevated water temperature reduces the acute toxicity of the widely used herbicide diuron to a green alga, Pseudokirchneriella subcapitata. Environ Sci Pollut Res Int 21:1064–1070CrossRefGoogle Scholar
  66. Vavilala SL, Sinha M, Gawde KK, Shirolikar SM, D'Souza JS (2016) KCl induces a caspase-independent programmed cell death in the unicellular green chlorophyte Chlamydomonas reinhardtii (Chlorophyceae). Phycologia 55:378–392CrossRefGoogle Scholar
  67. Vega FA, Covelo EF, Andrade ML (2007) Accidental organochlorine pesticide contamination of soil in Porriño, Spain. J Environ Qual 36:272–279CrossRefGoogle Scholar
  68. Vonberg D, Vanderborght J, Cremer N, Pütz T, Herbst M, Vereecken H (2014) 20 years of long-term atrazine monitoring in a shallow aquifer in western Germany. Water Res 50:294–306CrossRefGoogle Scholar
  69. Wolfe M, Seiber J (1993) Environmental activation of pesticides. Occup Med (Philadelphia, Pa) 8:561–573Google Scholar
  70. Yamagishi T, Horie Y, Tatarazako N (2017) Synergism between macrolide antibiotics and the azole fungicide ketoconazole in growth inhibition testing of the green alga Pseudokirchneriella subcapitata. Chemosphere 174:1–7CrossRefGoogle Scholar
  71. Yeo BS, Chu WL, Wong CY, Kok YY, Phang SM, Tan BK, Mustafa EM (2018) Combined effects of glufosinate ammonium and temperature on the growth, photosynthetic pigment content and oxidative stress response of Chlorella sp. and Pseudokirchneriella subcapitata. J Appl Phycol 30:3043–3055CrossRefGoogle Scholar
  72. Zakaria Z, Heng LY, Abdullah P, Osman R, Din L (2003) The environmental contamination by organochlorine insecticides of some agricultural areas in Malaysia. Malay J Chem 5:78–85Google Scholar
  73. Zhang W, Jiang F, Ou J (2011) Global pesticide consumption and pollution: with China as a focus. Proceed Int Acad Ecol Environ Sci 1:125Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Yin-Yien Chin
    • 1
  • Wan-Loy Chu
    • 1
    • 2
    Email author
  • Yih-Yih Kok
    • 3
  • Siew-Moi Phang
    • 4
  • Chiew-Yen Wong
    • 3
  • Boon-Keat Tan
    • 2
  • Emienour Muzalina Mustafa
    • 5
  1. 1.School of Postgraduate StudiesInternational Medical UniversityKuala LumpurMalaysia
  2. 2.Division of Human Biology, School of MedicineInternational Medical UniversityKuala LumpurMalaysia
  3. 3.Division of Applied Biomedical Sciences and Biotechnology, School of Health SciencesInternational Medical UniversityKuala LumpurMalaysia
  4. 4.Institute of Biological Sciences & Institute of Ocean and Earth SciencesUniversity of MalayaKuala LumpurMalaysia
  5. 5.School of Fisheries and Aquaculture SciencesUniversiti Malaysia TerengganuKuala TerengganuMalaysia

Personalised recommendations