Skip to main content

Advertisement

Log in

Azoxystrobin-induced excessive reactive oxygen species (ROS) production and inhibition of photosynthesis in the unicellular green algae Chlorella vulgaris

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

This study investigated the short-term toxicity of azoxystrobin (AZ), one of strobilurins used as an effective fungicidal agent to control the Asian soybean rust, on aquatic unicellular algae Chlorella vulgaris. The median percentile inhibition concentration (IC50) of AZ for C. vulgaris was found to be 510 μg L−1. We showed that the algal cells were obviously depressed or shrunk in 300 and 600 μg L−1 AZ treatments by using the electron microscopy. Furthermore, 19, 75, and 300 μg L−1 AZ treatments decreased the soluble protein content and chlorophyll concentrations in C. vulgaris and altered the energy-photosynthesis-related mRNA expression levels in 48- and 96-h exposure periods. Simultaneously, our results showed that AZ could increase the total antioxidant capacity (T-AOC) level and compromise superoxide dismutase (SOD), peroxidase (POD), glutathione S transferase (GST), glutathione peroxidase (GPx) activities, and glutathione (GSH) content. These situations might render C. vulgaris more vulnerable to oxidative damage. Overall, the present study indicated that AZ might be toxic to the growth of C. vulgaris, affect energy-photosynthesis-related mRNA expressions, and induce reactive oxygen species (ROS) overproduction in C. vulgaris.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B (2002) The strobilurin fungicides. Pest Manag Sci 58:649–662

    Article  CAS  Google Scholar 

  • Berenzen N, Lentzen-Godding A, Probst M, Schulz H, Schulz R, Liess M (2005) A comparison of predicted and measured levels of runoff-related pesticide concentrations in small lowland streams on a landscape level. Chemosphere 58:683–691

    Article  CAS  Google Scholar 

  • Bernal M, Sánchez-Testillano P, del Carmen Risueño M, Yruela I (2006) Excess copper induces structural changes in cultured photosynthetic soybean cells. Funct Plant Biol 33:1001–1012

    Article  CAS  Google Scholar 

  • Björkman O (1981) Responses to different quantum flux densities [M]//physiological plant ecology I. Springer, Berlin, pp 57–107

    Google Scholar 

  • Blaise C (1993) Practical laboratory applications with micro-algae for hazard assessment of aquatic contaminants. Ecotoxicology Monitoring, VCH Publishers, Weinheim, pp 83–107

    Google Scholar 

  • Blaise C, Vasseur P (2005) Algal microplate toxicity test. Small-scale freshwater toxicity investigations. Springer, p 137–179

  • Bornman JF, Vogelmann TC (1991) Effect of UV-B radiation on leaf optical properties measured with fiber optics. J Exp Bot 42:547–554

    Article  Google Scholar 

  • 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 72:248–254

    Article  CAS  Google Scholar 

  • El-Demerdash FM (2011) Lipid peroxidation, oxidative stress and acetylcholinesterase in rat brain exposed to organophosphate and pyrethroid insecticides. Food Chem Toxicol 49:1346–1352

    Article  CAS  Google Scholar 

  • European Food Safety Authority (EFSA) (2010) Peer review report to the conclusion regarding the peer review of the pesticide risk assessment of the active substance azoxystrobin. EFSA J 8:1542

    Google Scholar 

  • Fernández-Dávila ML, Razo-Estrada AC, García-Medina S, Gómez-Oliván LM, Piñón-López MJ, Ibarra RG, Galar-Martínez M (2012) Aluminum-induced oxidative stress and neurotoxicity in grass carp (Cyprinidae—Ctenopharingodon idella). Ecotoxicol Environ Saf 76:87–92

    Article  Google Scholar 

  • Fetoui H, Garoui EM, Zeghal E (2009) Lambda-cyhalothrin-induced biochemical and histopathological changes in the liver of rats: ameliorative effect of ascorbic acid. Exp Toxicol Pathol 61:189–196

    Article  CAS  Google Scholar 

  • Geret F, Bebianno MJ (2004) Does zinc produce reactive oxygen species in Ruditapes decussatus? Ecotoxicol Environ Saf 57:399–409

    Article  CAS  Google Scholar 

  • Gustafsson K, Blidberg E, Elfgren IK, Hellström A, Kylin H, Gorokhova E (2010) Direct and indirect effects of the fungicide azoxystrobin in outdoor brackish water microcosms. Ecotoxicology 19:431–444

    Article  CAS  Google Scholar 

  • Hnatova M, Gbelska Y, Obernauerova M, Šubíková V, Šubík J (2003) Cross-resistance to strobilurin fungicides in mitochondrial and nuclear mutants of Saccharomyces cerevisiae. Folia Microbiol 48:496–500

    Article  CAS  Google Scholar 

  • Hooser EA, Belden JB, Smith LM, McMurry ST (2012) Acute toxicity of three strobilurin fungicide formulations and their active ingredients to tadpoles. Ecotoxicology 21:1458–1464

    Article  CAS  Google Scholar 

  • Hörnström E (1990) Toxicity test with algae—a discussion on the batch method. Ecotoxicol Environ Saf 20:343–353

    Article  Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485

    Article  CAS  Google Scholar 

  • Jorgensen LF, Kjaer J, Olsen P, Rosenbom AE (2012) Leaching of azoxystrobin and its degradation product R234886 from Danish agricultural field sites. Chemosphere 88:554–562

    Article  Google Scholar 

  • Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78

    Article  CAS  Google Scholar 

  • Liess M, Ohe PCVD (2005) Analyzing effects of pesticides on invertebrate communities in streams. Environ Toxicol Chem 24:954–965

    Article  CAS  Google Scholar 

  • Liu L, Jiang C, Wu ZQ, Gong YX, Wang GX (2013) Toxic effects of three strobilurins (trifloxystrobin, azoxystrobin and kresoxim-methyl) on mRNA expression and antioxidant enzymes in grass carp (Ctenopharyngodon idella) juveniles. Ecotoxicol Environ Saf 98:297–302

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Lushchak VI, Bagnyukova TV (2007) Hypoxia induces oxidative stress in tissues of a goby, the rotan Perccottus glenii. Comp Biochem Physiol B 148:390–397

    Article  Google Scholar 

  • Maltby L, Brock TC, Van Den Brink PJ (2009) Fungicide risk assessment for aquatic ecosystems: importance of interspecific variation, toxic mode of action, and exposure regime. Environ Sci Technol 43:7556–7563

    Article  CAS  Google Scholar 

  • Mansour SA, Mossa ATH (2009) Lipid peroxidation and oxidative stress in rat erythrocytes induced by chlorpyrifos and the protective effect of zinc. Pestic Biochem Physiol 93:34–39

    Article  CAS  Google Scholar 

  • Ochoa-Acuña HG, Bialkowski W, Yale G, Hahn L (2009) Toxicity of soybean rust fungicides to freshwater algae and Daphnia magna. Ecotoxicology 18:440–446

    Article  Google Scholar 

  • Qian HF, Sheng GD, 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 27:182–187

    Article  CAS  Google Scholar 

  • Qian HF, Chen W, Sun L, Jin Y, Liu W, Fu Z (2009a) Inhibitory effects of paraquat on photosynthesis and the response to oxidative stress in Chlorella vulgaris. Ecotoxicology 18:537–543

    Article  CAS  Google Scholar 

  • Qian HF, Xu XY, Chen W, Jiang H, Jin YX, Liu WP, Fu ZW (2009b) Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 75:368–375

    Article  CAS  Google Scholar 

  • Qian HF, Li J, Pan XJ, Chen J, Zhou DM, Chen ZG, Zhang L, Fu ZW (2012) Analyses of gene expression and physiological changes in Microcystis aeruginosa reveal the phytotoxicities of three environmental pollutants. Ecotoxicology 3:847–859

    Article  Google Scholar 

  • Rippka R (1972) Photoheterotrophy and chemoheterotrophy among unicellular blue-green algae. Arch Mikrobiol 87:93–98

    Article  Google Scholar 

  • Rodrigues ET, Lopes I, Pardal MÂ (2013) Occurrence, fate and effects of azoxystrobin in aquatic ecosystems: a review. Environ Int 53:18–28

    Article  CAS  Google Scholar 

  • Shen YF, Liu L, Gong YX, Zhu B, Liu GL, Wang GX (2014) Potential toxic effect of trifloxystrobin on cellular microstructure, mRNA expression and antioxidant enzymes in Chlorella vulgaris. Environ Toxicol Pharmacol 37:1040–1047

    Article  CAS  Google Scholar 

  • Tate JJ, Gutierrez-Wing MT, Rusch KA, Benton MG (2012) Gene expression analysis of a Louisiana native Chlorella vulgaris (Chlorophyta)/Leptolyngbya sp. (Cyanobacteria) co-culture using suppression subtractive hybridization. Eng Life Sci 13:185–193

    Article  Google Scholar 

  • United States Environmental Protection Agency (US-EPA) (1997) Pesticide fact sheet. http://www.epa.gov/opp00001/chem_search/reg_actions/registration/fs_PC-128810_07-Feb-97.pdf

  • United States Environmental Protection Agency (US-EPA) (2012) ECOTOX user guide. http://cfpub.epa.gov/ecotox/blackbox/help/userhelp4.pdf

  • Van Rensburg S, Carstens M, Potocnik F, Van Der Spuy G, Van Der Walt B, Taljaard J (1995) Transferrin C2 and Alzheimer’s disease: another piece of the puzzle found? Med Hypotheses 44:268–272

    Article  Google Scholar 

  • Xia Z, Lundgren B, Bergstrand A, DePierre JW, Nässberger L (1999) Changes in the generation of reactive oxygen species and in mitochondrial membrane potential during apoptosis induced by the antidepressants imipramine, clomipramine, and citalopram and the effects on these changes by Bcl-2 and Bcl-X (L). Biochem Pharmacol 57:1199–1208

    Article  CAS  Google Scholar 

  • Zafar MI, Belgers JDM, Van Wijngaarden RP, Matser A, Van den Brink PJ (2012) Ecological impacts of time-variable exposure regimes to the fungicide azoxystrobin on freshwater communities in outdoor microcosms. Ecotoxicology 21:1024–1038

    Article  CAS  Google Scholar 

  • Zhu B, Liu GL, Liu L, Ling F, Wang GX (2015) Assessment of trifloxystrobin uptake kinetics, developmental toxicity and mRNA expression in rare minnow embryos. Chemosphere 120:447–455

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gao-Xue Wang.

Additional information

Responsible editor: Henner Hollert

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, L., Zhu, B. & Wang, GX. Azoxystrobin-induced excessive reactive oxygen species (ROS) production and inhibition of photosynthesis in the unicellular green algae Chlorella vulgaris . Environ Sci Pollut Res 22, 7766–7775 (2015). https://doi.org/10.1007/s11356-015-4121-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4121-7

Keywords