Abstract
Only limited information is available on herbicide toxicity to algae under mixotrophic conditions. In the present study, we studied the effects of the herbicide paraquat on growth, photosynthetic pigments, antioxidant enzymes, and gene expression in Chlorella pyrenoidosa under mixotrophic compared with autotrophic conditions. The mean measured exposure concentrations of paraquat under mixotrophic and autotrophic conditions were in the range of 0.3–3.4 and 0.6–3.6 μM, respectively. Exposure to paraquat for 72 h under both autotrophic and mixotrophic conditions induced decreased growth and chlorophyll (Chl) content, increased superoxide dismutase and peroxidase activities, and decreased transcript abundances of three photosynthesis-related genes (light-independent protochlorophyllide reductase subunit, photosystem II protein D1, and ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit [rbcL]). Compared with autotrophic conditions, the inhibition percentage of growth rate under mixotrophic conditions was lower at 0.8 μM paraquat, whereas it was greater at 1.8 and 3.4 μM paraquat. With exposure to 0.8–3.4 μM paraquat, the inhibition rates of Chl a and b content under mixotrophic conditions (43.1–52.4 % and 54.6–59.7 %, respectively) were greater compared with autotrophic conditions, whereas the inhibition rate of rbcL gene transcription under mixotrophic conditions (35.7–44.0 %) was lower. These data showed that similar to autotrophic conditions, paraquat affected the activities of antioxidant enzymes and decreased Chl synthesis and transcription of photosynthesis-related genes in C. pyrenoidosa under mixotrophic conditions, but a differential susceptibility to paraquat toxicity occurred between autotrophically versus mixotrophically grown cells.
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References
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
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 46:24–31
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
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
Cheng J, Huang Y, Feng J, Sun J, Zhou JH, Cen KF (2013) Mutate Chlorella sp. by nuclear irradiation to fix high concentrations of CO2. Bioresour Technol 136:496–501
Eullaffroy P, Vernet G (2003) The F684/F735 chlorophyll fluorescence ratio: a potential tool for rapid detection and determination of herbicide phytotoxicity in algae. Water Res 37:1983–1990
Franqueira D, Cid A, Torres E, Orosa M, Herrero C (1999) A comparison of the relative sensitivity of structural and functional cellular responses in the alga Chlamydomonas eugametos exposed to the herbicide paraquat. Arch Environ Contam Toxicol 36:264–269
Fuerst EP, Vaughn KC (1990) Mechanisms of paraquat resistance. Weed Technol 4:150–156
Gaydon DS, Probert ME, Buresh RJ, Meinke H, Timsina J (2012) Modelling the role of algae in rice crop nutrition and soil organic carbon maintenance. Eur J Agron 39:35–43
Goldschmidt-Clermont M (1986) The two genes for the small subunit of RuBp carboxylase/oxygenase are closely linked in Chlamydomonas reinhardtii. Plant Mol Biol 6:13–21
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485
Jamers A, De Coen W (2010) Effect assessment of the herbicide paraquat on a green alga using differential gene expression and biochemical biomarkers. Environ Toxicol Chem 29:893–901
Kamjunke N, Köhler B, Wannicke N (2008) Algae as competitors for glucose with heterotrophic bacteria. J Phycol 44:616–623
Kindle KL (1987) Expression of a gene for a light-harvesting chlorophyll a/b-binding protein in Chlamydomonas reinhardtii: effect of light and acetate. Plant Mol Biol 9:547–563
Leboulanger C, Bouvy M, Pagano M, Dufour R, Got P, Cecchi P (2009) Responses of planktonic microorganisms from tropical reservoirs to paraquat and deltamethrin exposure. Arch Environ Contam Toxicol 56:39–51
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
Megharaj M, Venkateswarlu K, Naidu R (2011) Effects of carbaryl and 1-naphthol on soil population of cyanobacteria and microalgae and select cultures of diazotrophic cyanobacteria. Bull Environ Contam Toxicol 87:324–329
Montavon P, Bortlik K (2004) Evolution of robusta green coffee redox enzymatic activities with maturation. J Agric Food Chem 52:3590–3594
Muraki N, Nomata J, Ebata K, Mizoguchi T, Shiba T, Tamiaki H et al (2010) X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature 456:110–115
Paixão P, Costa P, Bugalho T, Fidalgo C, Pereira LM (2002) Simple method for determination of paraquat in plasma and serum of human patients by high-performance liquid chromatography. J Chromatogr B 775:109–113
Pimentel D (1995) Amounts of pesticides reaching target pests: environmental impacts and ethics. J Agric Environ Ethics 8:17–29
Prado R, Rioboo C, Herrero C, Cid A (2009) The herbicide paraquat induces alterations in the elemental and biochemical composition of non-target microalgal species. Chemosphere 76:1440–1444
Qian HF, Chen W, Sun LW, Jin YX, Liu WP, Fu ZW (2009) Inhibitory effects of paraquat on photosynthesis and the response to oxidative stress in Chlorella vulgaris. Ecotoxicology 18:537–543
Reisser W (2007) The hidden life of algae underground. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Netherlands, pp 49–60
Rioboo C, Prado R, Herrero C, Cid A (2007) Population growth study of the rotifer Brachionus sp. fed with triazine-exposed microalgae. Aquat Toxicol 83:247–253
Shimmel SM, Darley WM (1985) Productivity and density of soil algae in an agricultural system. Ecology 66:1439–1447
Suntres ZE (2002) Role of antioxidants in paraquat toxicity. Toxicology 180:65–77
Valverde F, Ortega JM, Losada M, Serrano A (2005) Sugar-mediated transcriptional regulation of the Gap gene system and concerted photosystem II functional modulation in the microalga Scenedesmus vacuolatus. Planta 221:937–952
Villarejo A, Orús MI, Martínez F (1995) Coordination of photosynthetic and respiratory metabolism in Chlorella vulgaris UAM 101 in the light. Physiol Plant 94:680–686
Wang HY, Xiong HR, Hui ZL, Zeng XB (2012) Mixotrophic cultivation of Chlorella pyrenoidosa with diluted primary piggery wastewater to produce lipids. Bioresour Technol 104:215–220
Wetzel RG (2001) Limnology, 3rd edn. Academic, San Diego
Wong PK (2000) Effects of 2,4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll-a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere 41:177–182
Yan GA, Yan X, Wu W (1997) Effects of the herbicide molinate on mixotrophic growth, photosynthetic pigments, and protein content of Anabaena sphaerica under different light conditions. Ecotoxicol Environ Saf 38:144–149
Zancan S, Trevisan R, Paoletti MG (2006) Soil algae composition under different agro-ecosystems in North-Eastern Italy. Agric Ecosyst Environ 112:1–12
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The authors thank the reviewers and editors for their valuable comments to improve this manuscript. This study was financially supported by National Environmental Protection Public Welfare Science and Technology Research Program of China (Grant No. 201009033) and the National Natural Science Foundation of China (Grant No. 31270447).
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Zhang, W., Liu, M., Zhang, P. et al. Effects of Paraquat on Photosynthetic Pigments, Antioxidant Enzymes, and Gene Expression in Chlorella pyrenoidosa Under Mixotrophic Compared With Autotrophic Conditions. Arch Environ Contam Toxicol 67, 593–600 (2014). https://doi.org/10.1007/s00244-014-0067-x
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DOI: https://doi.org/10.1007/s00244-014-0067-x