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Disturbance of chiral ionic liquids to phototaxis of Chlamydomonas reinhardtii: regular analysis and mechanism attempt

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Abstract

Given the recent extensive synthesis and application of ionic liquids (ILs), finding a sensitive and visual indicator to provide a fast-initial risk assessment of IL use has become a pressing issue. In this study, we verified that the phototaxis of Chlamydomonas reinhardtii is a valid indicator of the environmental risk associated with chiral ILs L-(+)- and D-(−)-1-butyl-3-methylimidazolium lactate (BMIM L). Briefly, C. reinhardtii was exposed to a 4000-lx side light source for varying lengths of time. Following the allotted exposure time, the algae aggregation was photographed, and then quantitative analysis was conducted using Image-J software to obtain the corresponding relationship between IL stimulation and C. reinhardtii phototaxis. The gray areas from each treatment were measured and the percentage was calculated. After 16 h of side lighting, for control, the percentage of gray areas was − 22%, while for L-(+)- and D-(−)- BMIM L were 17% and 33%, respectively. Then, after 8 h of darkness, where D-(−)-BMIM L and the control showed the positive phototaxis, but the L-(+)-BMIM L-treated group showed virtually no change. This phenomenon is consistent with excessive production of reactive oxygen species (ROS). Moreover, atomic force microscope (AFM) results indicated distinct aggregation between D-(−)- and L-(+)-BMIM L, which caused changes in cell permeability that induced a change in ROS transfer. Furthermore, relationship between phototaxis and changes in cell ultrastructure and photosynthetic efficiency was also investigated. This work demonstrates the potential of phototaxis to serve as a sensitive, convenient, and cost effective qualitative assessment of ILs’ toxic impact, with the understanding that quantitative evaluation requires further improvement.

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References

  • Arrieta J, Barreira A, Chioccioli M, Polin M, Tuval I (2017) Phototaxis beyond turning: persistent accumulation and response acclimation of the microalga Chlamydomonas reinhardtii. Scientific Reports 7 (1)

  • Bartolome MC, Sanchez-Fortun S (2005) Acute toxicity and inhibition of phototaxis induced by benzalkonium chloride in Artemia franciscana larvae. Bull Environ Contam Toxicol 75:1208–1213

    CAS  Google Scholar 

  • Biedron T, Kubisa P (2005) Radical polymerization in a chiral ionic liquid: atom transfer radical polymerization of acrylates. J Polym Sci A Polym Chem 43:3454–3459

    CAS  Google Scholar 

  • Bubalo M C, Radošević K, Redovniković, Halambek I R, J. Srček V G (2014) A brief overview of the potential environmental hazards of ionic liquids. Ecotox Environ Safe 99: 1–12

  • Cao LD, Zhu P, Zhao YS, Zhao JH (2018) Using machine learning and quantum chemistry descriptors to predict the toxicity of ionic liquids. J Hazard Mater 352:17–26

    CAS  Google Scholar 

  • Chen H, Sheng XL, Wen YZ, Zhang LJ, Bao HL, Li LN, Liu WP (2013) New insights into the effects of the herbicide imazethapyr on Cu(II) ecotoxicity to the aquatic unicellular alga Scenedesmus obliquus. Aquat Toxicol 140-141:407–414

    CAS  Google Scholar 

  • Chen H, Zou YQ, Zhang LJ, Wen YZ, Liu WP (2014) Enantioselective toxicities of chiral ionic liquids 1-alkyl-3-methylimidazolium lactate to aquatic algae. Aquat Toxicol 154:114–120

    CAS  Google Scholar 

  • Chen ZW, Wang J, Chen H, Wen YZ, Liu WP (2017) Enantioselective phytotoxicity of dichlorprop to Arabidopsis thaliana: the effect of cytochrome P450 enzymes and the role of Fe. Environ Sci Technol 51(20):12007–12015

    CAS  Google Scholar 

  • Chen SY, Chen H, Chen ZW, Wen YZ, Liu WP (2019a) Enantioselective phytotoxic disturbances of fatty acids in Arabidopsis thaliana by dichlorprop. Environ Sci Technol 53(15):9252–9259

    CAS  Google Scholar 

  • Chen SY, Zhang LJ, Chen H, Chen ZW, Wen YZ (2019b) Enantioselective toxicity of chiral herbicide metolachlor to Microcystis aeruginosa. J Agric Food Chem 67:1631–1637

    CAS  Google Scholar 

  • Diaz E, Monsalvo VM, Lopez J, Mena IF, Palomar J, Rodriguez JJ, Mohedano AF (2018) Assessment the ecotoxicity and inhibition of imidazolium ionic liquids by respiration inhibition assays. Ecotox Environ Safe 162:29–34

    CAS  Google Scholar 

  • Drescher K, Goldstein RE, Tuval I (2010) Fidelity of adaptive phototaxis. P Natl Acad Sci USA 107:11171–11176

    CAS  Google Scholar 

  • Fan HY, Jin MK, Wang H, Xu QR, Xu L, Wang CX, Du ST, Liu HJ (2019) Effect of differently methyl-substituted ionic liquids on Scenedesmus obliquus growth, photosynthesis, respiration, and ultrastructure. Environ Pollut 250:155–165

    CAS  Google Scholar 

  • Garcia X, Rafaï S, Peyla P (2013) Light control of the flow of phototactic microswimmer suspensions. Phys Rev Lett 110(13):138106

    Google Scholar 

  • Ghanem OB, Mutalib MA, El-Harbawi M, Gonfa G, Kait CF, Alitheen NBM, Leveque JM (2015) Effect of imidazolium-based ionic liquids on bacterial growth inhibition investigated via experimental and QSAR modelling studies. J Hazard Mater 297:198–206

    Google Scholar 

  • Giometto A, Altermatt F, Maritan A, Stocker R, Rinaldo A (2015) Generalized receptor law governs phototaxis in the phytoplankton Euglena gracilis. Proc Natl Acad Sci U S A 112(22):7045–7050

    CAS  Google Scholar 

  • Jin MK, Wang H, Li Z, Fu LY, Chu LL, Wu J, Du ST, Liu HJ (2019) Physiological responses of Chlorella pyrenoidosa to 1-hexyl-3-methyl chloride ionic liquids with different cations. Sci Total Environ 685:315–323

    CAS  Google Scholar 

  • Katano T, Yoshida M, Yamaguchi S, Yoshino K, Hamada T, Koriyama M, Hayami Y (2014) Effect of nutrient concentration and salinity on diel vertical migration of Chattonella marina (Raphidophyceae). Mar Biol Res 10(10):1007–1018

    Google Scholar 

  • Ken-ichi W, Yuka M, Shota M, Ritsu K (2011) Reduction-oxidation poise regulates the sign of phototaxis in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 108(27):11280–11284

    Google Scholar 

  • Kim D, Watanabe M, Nakayasu Y, Kohata K (2005) Changes in O2- and H2O2 production by Chattonella antiqua during diel vertical migration under nutrient stratification. Aquat Microb Ecol 39:183–191

    Google Scholar 

  • Kingston MB (1999) Effect of light on vertical migration and photosynthesis of Euglena proxima (Euglenophyta). J Phycol 35(2):245–253

    Google Scholar 

  • Knauert S, Knauer K (2008) The role of reactive oxygen species in copper toxicity to two freshwater green algae. J Physiol 44:311–319

    CAS  Google Scholar 

  • Kumar KS, Dahms HU, Lee JS, Kim HC, Lee WC, Shin KH (2014) Algal photosynthetic responses to toxic metals and herbicides assessed by chlorophyll a fluorescence. Ecotox Environ Safe 104(2):51–71

    Google Scholar 

  • Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determinethe different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43(3):379–393

    CAS  Google Scholar 

  • Liu HJ, Xiong MY (2009) Comparative toxicity of racemic metolachlor and Smetolachlor to Chlorella pyrenoidosa. Aquat Toxicol 93:100–106

    CAS  Google Scholar 

  • Liu HJ, Zhang XQ, Chen CD, Zhu SM, Ma XJ (2015) Enantioselective toxicities of chiral ionic liquids 1-alkyl-3-methylimidazolium tartrate on Scenedesmus obliquus. Aquat Toxicol 169:179–187

    CAS  Google Scholar 

  • Liu HJ, Wu J, Zhang XQ, Xia YL, Du ST (2017) Enantioselective oxidative stress caused by chiral ionic liquids forms of 1-alkyl-3-methyl imidazolium tartrate on Scenedesmus obliquus. Sci Total Environ 595:819–827

    CAS  Google Scholar 

  • Liu DD, Liu HJ, Wang ST, Chen JZ, Xia YL (2018) The toxicity of ionic liquid 1-decylpyridinium bromide to the algae Scenedesmus obliquus: growth inhibition, phototoxicity, and oxidative stress. Sci Total Environ 622-623:1572–1580

    CAS  Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666

    CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668

    CAS  Google Scholar 

  • Mehdi MM, Tabassom SA, Mahbobeh V, Mohammad AF (2017) Ionic liquids and their toxicity on the enzyme activity and stability. Tre Pep Pro Sci 2(1):24–34

    Google Scholar 

  • Moldrup M, Anders G (2012) Spectral sensitivity of phototaxis in the dinoflagellate Kryptoperidinium foliaceum and their reaction to physical encounters. J Exp Biol 215:2342–2346

    CAS  Google Scholar 

  • Montalban MG, Hidalgo JM, Collado-Gonzalez M, Banos FGD, Víllora G (2016) Assessing chemical toxicity of ionic liquids on Vibrio fischeri: correlation with structure and composition. Chemosphere 155:405–414

    CAS  Google Scholar 

  • Mouhamed N, David B, Tri NQ, Rene K, David H, Marie LB, Michele P, Sarah D (2017) A novel Eulerian approach for modelling cyanobacteria movement: thin layer formation and recurrent riskto drinking water intakes. Water Res 127:191–203

    Google Scholar 

  • Ooka H, Ishii T, Hashimoto K, Nakamura R (2014) Light-induced cell aggregation of Euglena gracilis towards economically feasible biofuel production. RSC Adv 4(40):20693–20698

    CAS  Google Scholar 

  • Pham TPT, Cho CW, Yun YS (2010) Environmental fate and toxicity of ionic liquids: a review. Water Res 44:352–372

    CAS  Google Scholar 

  • Pretti C, Chiappe C, Baldetti I, Brunini S, Monni G, Intorre L (2009) Acute toxicity of ionic liquids for three fresh water organisms: Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Ecotox Environ Safe 72:1170–1176

    CAS  Google Scholar 

  • Schulz PS, Muller N, Bosmann A, Wasserscheid P (2007) Effective chirality transfer in ionic liquids through ion-pairing effects. Angew Chem Int Ed 46:1293–1295

    CAS  Google Scholar 

  • Sengupta A, Carrara F, Stocker R (2017) Phytoplankton can actively diversify their migration strategy in response to turbulent cues. Nature:543–555

  • Shikata T, Matsunaga S, Kuwahara Y, Iwahori S, Nishiyama Y (2016) Light spectrum regulates cell accumulation during daytime in the raphidophyte Chattonella antiqua causing noxious red tides. J Photochem Photobiol B 160:128–133

    CAS  Google Scholar 

  • Shota M, Ken-ichi W (2012) Redox regulation of phototactic migration in the green alga Chlamydomonas reinhardtii and its possible application. Communi Integr Bio 5(2):196–198

    Google Scholar 

  • Sineshchekov OA, Jung K-H, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardti. Proc Natl Acad Sci U S A 99:8689–8694

    CAS  Google Scholar 

  • Takuma O, Shunsuke I, Makoto I (2017) Statistics and stochastic models of an individual motion of photosensitive alga Euglena gracilis. J Phys Soc Jpn 86:074401

    Google Scholar 

  • Tomoyuki S, Shigeru M, Yusuke K, Sho I, Yoshitaka N (2016) Light spectrum regulates cell accumulation during daytime in the raphidophyte Chattonella antiqua causing noxious red tides. J Photoch Phitobio B 160:128–133

    Google Scholar 

  • Wen Y Z, Yuan Y L, Shen C S, Liu H J, Liu W P (2009) Spectroscopic investigations of the chiral interactions between lipase and the herbicide dichlorprop 21(3): 396-401

  • Wen YZ, Chen H, Shen CS, Zhao MR, Liu WP (2011) Enantioselectivity tuning of chiral herbicide dichlorprop by copper: roles of reactive oxygen species. Environ Sci Technol 45:4778–4784

    CAS  Google Scholar 

  • Wen YZ, Zhang LJ, Chen ZW, Sheng XL, Qiu JG, Xu DM (2016) Co-exposure of silver nanoparticles and chiral herbicide imazethapyr to Arabidopsis thaliana: enantioselective effects. Chemosphere 145:207–214

    CAS  Google Scholar 

  • Wu XD, Kong FX (2009) Effects of light and wind speed on the vertical distribution of Microcystis aeruginosa colonies of different sizes during a summer bloom. Int Rev Hydrobiol 94(3):258–266

    Google Scholar 

  • Zeng LX, He YJ, Dai ZF, Wang J, Cao Q, Zhang YL (2009) Chiral induction, memory, and amplification in porphyrin homoaggregates based on electrostatic interactions. ChemPhysChem 10:954–962

    CAS  Google Scholar 

  • Zhang A, Liu W, Wang L, Wen Y (2005) Characterization of Inclusion Complexation between Fenoxaprop- -ethyl and Cyclodextrin. Journal of Agricultural and Food Chemistry 53 (18):7193-7197

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (NSFC, No. 21876150 and 21677124), the Zhejiang Provincial Natural Science Foundation of China (No. LQ19B070002), the Zhejiang Provincial Education Department Foundation of China (No. Y201839092), the Ningbo Municipal Natural Science Foundation of China (No. 2018A610209 and 2017A610299), and K. C. Wong Magna Fund in Ningbo University.

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Correspondence to Yuezhong Wen.

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Chen, H., Shen, C., Chen, Z. et al. Disturbance of chiral ionic liquids to phototaxis of Chlamydomonas reinhardtii: regular analysis and mechanism attempt. Environ Sci Pollut Res 27, 15011–15019 (2020). https://doi.org/10.1007/s11356-020-07882-6

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