Skip to main content
Log in

Sensitivity of Scenedesmus obliquus and Microcystis aeruginosa to atrazine: effects of acclimation and mixed cultures, and their removal ability

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Atrazine is an herbicide frequently detected in watercourses that can affect the phytoplankton community, thus impacting the whole food chain. This study aims, firstly, to measure the sensitivity of monocultures of the green alga Scenedemus obliquus and toxic and non-toxic strains of the cyanobacteria Microcystis aeruginosa before, during and after a 30-day acclimation period to 0.1 µM of atrazine. Secondly, the sensitivity of S. obliquus and M. aeruginosa to atrazine in mixed cultures was evaluated. Finally, the ability of these strains to remove atrazine from the media was measured. We demonstrated that both strains of M. aeruginosa had higher growth rate-based EC50 values than S. obliquus when exposed to atrazine, even though their photosynthesis-based EC50 values were lower. After being exposed to 0.1 µM of atrazine for 1 month, only the photosynthesis-based EC50 of S. obliquus increased significantly. In mixed cultures, the growth rate of the non-toxic strain of M. aeruginosa was higher than S. obliquus at high concentrations of atrazine, resulting in a ratio of M. aeruginosa to total cell count of 0.6. This lower sensitivity might be related to the higher growth rate of cyanobacteria at low light intensity. Finally, a negligible fraction of atrazine was removed from the culture media by S. obliquus or M. aeruginosa over 6 days. These results bring new insights on the acclimation of some phytoplankton species to atrazine and its effect on the competition between S. obliquus and M. aeruginosa in mixed cultures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alva-Martínez, AF, Sarma, SSS, Nandini, S, (2004) Population growth of Daphnia pulex (Cladocera) on a mixed diet (Microcystis aeruginosa with Chlorella or Scenedesmus). Crustaceana 77:973–988. http://www.jstor.org/stable/20105779

  • Bendall DS, Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochimica et Biophysica Acta Bioenergetics 1229:23–38. doi:10.1016/0005-2728(94)00195-B

    Article  Google Scholar 

  • Bérard A, Leboulanger S, 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 37:472–479. doi:10.1007/s002449900541

    Article  Google Scholar 

  • Campos MMC, Faria VHF, Teodoro TS, Barbosa FAR, Magalhães SMS (2013) Evaluation of the capacity of the cyanobacterium Microcystis novacekii to remove atrazine from a culture medium. J Environ Sci Health Part B 48:101–107. doi:10.1080/15226514.2010.52554910.1080/03601234.2013.726891

    Article  CAS  Google Scholar 

  • Caux P-Y, Kent RA (1995) Towards the development of site-specific water quality objective for atrazine in the Yamaska river, Quebec, for the protection of aquatic life. Water Qual Res J Can 30:157–178. doi:10.1016/j.aquatox.2012.09.005

    CAS  Google Scholar 

  • Cepoi L, Dontu N, Salaru V, Salaru V (2016) Removal of organic pollutants from wastewater by cyanobacteria. In: Zinicovscaia I, Cepoi L (eds) Cyanobacteria for bioremediation of wastewaters. Springer International Publishing, pp 27–44

  • Chalifour A, Juneau P (2011) Temperature-dependent sensitivity of growth and photosynthesis of Scenedesmus obliquus, Navicula pelliculosa and two strains of Microcystis aeruginosa to the herbicide atrazine. Aquat Toxicol 103:9–17. doi:10.1016/j.aquatox.2011.01.016

    Article  CAS  Google Scholar 

  • Deblois CP, Dufresne K, Juneau P (2013) Response to variable light intensity in photoacclimated algae and cyanobacteria exposed to atrazine. Aquat Toxicol 126:77–84. doi:10.1016/j.aquatox.2012.09.005

    Article  CAS  Google Scholar 

  • Deblois CP, Juneau P (2012) Comparison of resistance to light stress in toxic and non-toxic strains of Microcystis aeruginosa (Cyanophyta). J Phycol 48:1002–1011. doi:10.1111/j.1529-8817.2012.01191.x

    Article  CAS  Google Scholar 

  • Devilla RA, Brown MT, Donkin M, Readman JW (2005) The effects of a PSII inhibitor on phytoplankton community structure as assessed by HPLC pigment analyses, microscopy and flow cytometry. Aquat Toxicol 71:25–38. doi:10.1016/j.aquatox.2004.10.002

    Article  CAS  Google Scholar 

  • Dosnon-Olette R, Couderchet M, Oturan MA, Oturan N, Eullaffroy P (2011) Potential use of Lemna minor for the phytoremediation of isoproturon and glyphosate. Int J Phytoremediation 13:601–612. doi:10.1080/15226514.2010.525549

    Article  CAS  Google Scholar 

  • Fedtke C, Duke SO (2004) Herbicides. In: Hock B, Elstner EF (eds) Plant toxicology, 4th edn, CRC Press, New York, pp 247–330

  • García-Villada L, Reboud X (2007) Induction of atrazine tolerance in a natural soil assemblage of microalgae reared in the laboratory. Ecotoxicol Environ Saf 66:102–106. doi:10.1016/j.ecoenv.2005.09.003

    Article  Google Scholar 

  • Giroux I (2015) Présence de pesticides dans l’eau au Québec: portrait et tendances dans les zones de maïs et de soya—2011 à 2014, ISBN 978-2-550-73603-5, Québec, 47 pp and 43 annexes

  • González R, García-Balboa C, Rouco M, Lopez-Rodas V, Costas E (2012) Adaptation of microalgae to lindane: a new approach for bioremediation. Aquat Toxicol 109:25–32. doi:10.1016/j.aquatox.2011.11.015

    Article  Google Scholar 

  • González-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  Google Scholar 

  • Graymore M, Stagnitti F, Allinson G (2001) Impacts of atrazine in aquatic ecosystems. Environ Int 26:483–495. doi:10.1016/S0160-4120(01)00031-9

    Article  CAS  Google Scholar 

  • Huertas IE, Rouco M, López-Rodas V, Costas E (2010) Estimating the capability of different phytoplankton groups to adapt to contamination: herbicides will affect phytoplankton species differently. New Phytol 188:478–487. doi:10.1111/j.1469-8137.2010.03370.x

    Article  CAS  Google Scholar 

  • Jakob T, Schreiber U, Kirchesch V, Langner U, Wilhelm C (2005) Estimation of chlorophyll content and daily primary production of the major algal groups by means of multiwavelength-excitation PAM chlorophyll fluorometry: performance and methodological limits. Photosynth Res 83:343–361. doi:10.1007/s11120-005-1329-2

    Article  CAS  Google Scholar 

  • Kasai F (1999) Shifts in herbicide tolerance in paddy field periphyton following herbicide application. Chemosphere 38:919–931. doi:10.1016/S0045-6535(98)00221-5

    Article  CAS  Google Scholar 

  • Lockert CK, Hoagland KD, Siegfried BD (2006) Comparative sensitivity of freshwater algae to atrazine. Bull Environ Contam Toxicol 76:73–79. doi:10.1007/s00128-005-0891-9

    Article  CAS  Google Scholar 

  • Lürling M, Roessink I (2006) On the way to cyanobacterial blooms: impact of the herbicide metribuzin on the competition between a green alga (Scenedesmus) and a cyanobacterium (Microcystis). Chemosphere 65:618–626. doi:10.1016/j.chemosphere.2006.01.073

    Article  Google Scholar 

  • Marvá F, López-Rodas V, Rouco M, Navarro M, Toro FJ, Costas E, Flores-Moya A (2010) Adaptation of green microalgae to the herbicides simazine and diquat as result of pre-selective mutations. Aquat Toxicol 96:130–134. doi:10.1016/j.aquatox.2009.10.009

    Article  Google Scholar 

  • Murdock JN, Shields Jr FD, Lizotte Jr RE (2013) Periphyton responses to nutrient and atrazine mixtures introduced through agricultural runoff. Ecotoxicology 22:215–230. doi:10.1007/s10646-012-1018-9

    Article  CAS  Google Scholar 

  • Nelson KJ, Hoagland KD, Siegfried BD (1999) Chronic effects of atrazine on tolerance of a benthic diatom. Environ Toxicol Chem 18:1038–1045. http://digitalcommons.unl.edu/entomologyfacpub/54

  • Pannard A, Le Rouzic B, Binet F (2009) Response of phytoplankton community to low-dose atrazine exposure combined with phosphorus fluctuations. Arch Environ Contam Toxicol 57:50–59. doi:10.1007/s00244-008-9245-z

    Article  CAS  Google Scholar 

  • Peltier G, Tolleter D, Billon E, Cournac L (2010) Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth Res 106:19–31. doi:10.1007/s11120-010-9575-3

    Article  CAS  Google Scholar 

  • Pennington PL, Scott GI (2001) Toxicity of atrazine to the estuarine phytoplankter Pavlova sp. (Prymnesiophyceae): Increased sensitivity after long-term, low-level population exposure. Environ Toxicol Chem 20:2237–2242. doi:10.1002/etc.5620201016

    Article  CAS  Google Scholar 

  • Plumley FG, Davis D (1980) The effects of a photosynthesis inhibitor atrazine, on salt marsh edaphic algae, in culture, microecosystems, and in the field. Estuaries Coasts 3:271–277. doi:10.2307/1352082

    Article  CAS  Google Scholar 

  • Qian H, Tsuji T, Endo T, Sato F (2014) PGR5 and NDH pathways in photosynthetic cyclic electron transfer respond differently to sublethal treatment with photosystem-interfering herbicides. J Agric Food Chem 62:4083–4089. doi:10.1021/jf500143f

    Article  CAS  Google Scholar 

  • Sajjaphan K, Shapir N, Judd AK, Wackett LP, Sadowsky MJ (2002) Novel psbA1 gene from a naturally occurring atrazine-resistant cyanobacterial isolate. Appl Environ Microbiol 68:1358–1366. doi:10.1128/aem.68.3.1358-1366.2002

    Article  CAS  Google Scholar 

  • Schmitt-Jansen M, Altenburger R (2005a) Predicting and observing responses of algal communities to photosystem II-herbicide exposure using pollution-induced community tolerance and species-sensitivity distributions. Environ Toxicol Chem 24:304–312. doi:10.1897/03-647.1

    Article  CAS  Google Scholar 

  • Schmitt-Jansen M, Altenburger R (2005b) Toxic effects of isoproturon on periphyton communities - a microcosm study. Estuarine Coast Shelf Sci 62:539–545. doi:10.1016/j.ecss.2004.09.016

    Article  CAS  Google Scholar 

  • Schmitt-Jansen M, Altenburger R (2008) Community-level microalgal toxicity assessment by multiwavelength-excitation PAM fluorometry. Aquat Toxicol 86:49–58. doi:10.1016/j.aquatox.2007.10.001

    Article  CAS  Google Scholar 

  • 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 36:3227–3236. doi:10.1016/S0043-1354(02)00013-1

    Article  CAS  Google Scholar 

  • Stange K, Swackhamer DL (1994) Factors affecting phytoplankton species-specific differences in accumulation of 40 polychlorinated biphenyls (PCBs). Environ Toxicol Chem 13:1849–1860. doi:10.1002/etc.5620131117

    Article  CAS  Google Scholar 

  • Stein JR (1973) Culture methods and growth measurements. Cambridge University Press, Cambridge

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London, pp 443–480

  • Sullivan DJ, Vecchia AV, Lorenz DL, Gilliom RJ, Martin JD (2009) Trends in pesticide concentrations in corn-belt streams, 1996–2006: U.S. Geological Survey Scientific Investigations Report 2009-5132, 75 pp

  • 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%3C1085:UABOAB%3E2.3.CO;2

    Article  CAS  Google Scholar 

  • Tuckey DM, Orcutt DM, Hipkins PLL (2002) Inherent and growth stage-related differences in growth and lipid and sterol composition of algal species sensitive and tolerant to sterol-inhibiting fungicides. Environ Toxicol Chem 21:1715–1723. doi:10.1002/etc.5620210825

    CAS  Google Scholar 

  • Vermaas WF (2001) Photosynthesis and respiration in cyanobacteria. Encycl Life Sci 1–7. doi:10.1038/npg.els.0001670

  • Wang S, Zhang D, Pan X (2013) Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. Chemosphere 93:230–237. doi:10.1016/j.chemosphere.2013.04.070

    Article  CAS  Google Scholar 

  • Weiner JA, 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 

  • Weyman GS, Rufli H, Weltje L, Salinas ER, Hamitou M (2012) Aquatic toxicity tests with substances that are poorly soluble in water and consequences for environmental risk assessment. Environ Toxicol Chem 31:1662–1669. doi:10.1002/etc.1856

    Article  CAS  Google Scholar 

  • You L, He L, Tang YJ (2015) Photoheterotrophic fluxome in Synechocystis sp. strain PCC 6803 and its implications for cyanobacterial bioenergetics. J Bacteriol 197:943–950. doi:10.1128/jb.02149-14

    Article  Google Scholar 

  • Zablotowicz RM, Schrader KK, Locke MA (1998) Algal transformation of fluometuron and atrazine by N-dealkylation. J Environ Sci Health Part B 33:511–528. doi:10.1080/03601239809373160

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Stéphanie Potvin and Denis Flipo for her technical assistance in this project.

Funding

Financial support was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC, grant #262210–2011) awarded to PJ. AC received an Alexander-Graham-Bell scholarship from NSERC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Philippe Juneau.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chalifour, A., LeBlanc, A., Sleno, L. et al. Sensitivity of Scenedesmus obliquus and Microcystis aeruginosa to atrazine: effects of acclimation and mixed cultures, and their removal ability. Ecotoxicology 25, 1822–1831 (2016). https://doi.org/10.1007/s10646-016-1728-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-016-1728-5

Keywords

Navigation