Abstract
Introduction
Micropollutants are increasingly monitored as their presence in the environment is rising due to human activities, and they are potential threats to living organisms.
Objectives
This study aimed at understanding the role of plants in xenobiotics removal from polluted environments by following xenobiotics metabolism in leaf tissues.
Methods
Different classes of micropollutants were investigated using liquid chromatography (LC) coupled to quadrupole-time of flight (Q-TOF) high resolution mass spectrometry (HRMS). The tissue localization of xenobiotics in the leaves of a spontaneous (not planted by humans) Salix alba growing near the water flux was further investigated using matrix-assisted laser desorption ionization (MALDI) mass spectrometry imaging (MSI).
Results
The LC-Q-TOF analysis revealed the distribution of micropollutants in three different compartments of a tertiary treatment wetland. When further investing the metabolic profile of S. alba leaves using MSI, different distribution patterns were observed in specific leaf tissues. Xenobiotic metabolites were predicted and could also be tentatively identified in S. alba leaves, shedding new light on the metabolic processes at play in leaves to manage xenobiotics uptake from a polluted environment.
Conclusion
Using complementary metabolomics approaches, this study performed a large-scale exploration of micropollutants spreading in the environment at the exit of a tertiary treatment wetland. The use of MSI coupled with the prediction of xenobiotic metabolites yielded novel insights into plant metabolism during chronical exposure to low doses of a mixture of micropollutants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request.
References
Alygizakis, N. A., Gago-Ferrero, P., Borova, V. L., Pavlidou, A., Hatzianestis, I., & Thomaidis, N. S. (2016). Occurrence and spatial distribution of 158 pharmaceuticals, drugs of abuse and related metabolites in offshore seawater. Science of the Total Environment, 541, 1097–1105. https://doi.org/10.1016/j.scitotenv.2015.09.145.
Anderson, D. M. G., Carolan, V. A., Crosland, S., Sharples, K. R., & Clench, M. R. (2010). Examination of the translocation of sulfonylurea herbicides in sunflower plants by matrix-assisted laser desorption/ionisation mass spectrometry imaging. Rapid Communications in Mass Spectrometry, 24, 3309–3319. https://doi.org/10.1002/rcm.4767.
Bártíková, H., Skálová, L., Stuchlíková, L., Vokřál, I., Vaněk, T., & Podlipná, R. (2015). Xenobiotic-metabolizing enzymes in plants and their role in uptake and biotransformation of veterinary drugs in the environment. Drug Metabolism Reviews, 47(3), 374–387. https://doi.org/10.3109/03602532.2015.1076437.
Berthelot, C., Leyval, C., Foulon, J., Chalot, M., & Blaudez, D. (2016). Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiology Ecology, 92(10), fiw144. https://doi.org/10.1093/femsec/fiw144.
Boleda, M. R., Galceran, M. T., & Ventura, F. (2013). Validation and uncertainty estimation of a multiresidue method for pharmaceuticals in surface and treated waters by liquid chromatography-tandem mass spectrometry. Journal of Chromatography A, 1286, 146–158. https://doi.org/10.1016/j.chroma.2013.02.077.
Bucheli, T. D. (2014). Phytotoxins: Environmental micropollutants of concern? Environmental Science and Technology, 48, 13027–13033. https://doi.org/10.1021/es504342w.
Coleman, J. O. D., Blake-Kalff, M. M. A., & Davies, T. G. E. (1997). Detoxification of xenobiotics by plants: Chemical modification and vacuolar compartmentation. Trends in Plant Science, 2(4), 144–151. https://doi.org/10.1016/S1360-1385(97)01019-4.
Fernandes, C., Figueira, E., Tauler, R., & Bedia, C. (2018). Exposure to chlorpyrifos induces morphometric, biochemical and lipidomic alterations in green beans (Phaseolus vulgaris). Ecotoxicology and Environmental Safety, 156(March), 25–33. https://doi.org/10.1016/j.ecoenv.2018.03.005.
He, Y., Langenhoff, A. A. M., Sutton, N. B., Rijnaarts, H. H. M., Blokland, M. H., Chen, F., et al. (2017). Metabolism of ibuprofen by Phragmites australis: Uptake and phytodegradation. Environmental Science and Technology, 51(8), 4576–4584. https://doi.org/10.1021/acs.est.7b00458.
Huber, C., Bartha, B., Harpaintner, R., & Schröder, P. (2009). Metabolism of acetaminophen (paracetamol) in plants-two independent pathways result in the formation of a glutathione and a glucose conjugate. Environmental Science and Pollution Research, 16(2), 206–213. https://doi.org/10.1007/s11356-008-0095-z.
Klampfl, C. W. (2019). Metabolization of pharmaceuticals by plants after uptake from water and soil: A review. Trends in Analytical Chemistry, 111, 13–26. https://doi.org/10.1016/j.trac.2018.11.042.
Komives, T., & Gullner, G. (2005). Phase I xenobiotic metabolic systems in plants. Zeitschrift fur Naturforschung—Section C Journal of Biosciences, 60(3–4), 179–185.
Lagarrigue, M., Caprioli, R. M., & Pineau, C. (2016). Potential of MALDI imaging for the toxicological evaluation of environmental pollutants. Journal of Proteomics, 144, 133–139. https://doi.org/10.1016/j.jprot.2016.05.008.
Li, W. C., & Wong, M. H. (2012). Interaction of Cd/Zn hyperaccumulating plant (Sedum alfredii) and rhizosphere bacteria on metal uptake and removal of phenanthrene. Journal of Hazardous Materials, 209–210, 421–433. https://doi.org/10.1016/j.jhazmat.2012.01.055.
Ma, Y., Rajkumar, M., Zhang, C., & Freitas, H. (2016). Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management, 174, 14–25. https://doi.org/10.1016/j.jenvman.2016.02.047.
Marsik, P., Sisa, M., Lacina, O., Motkova, K., Langhansova, L., Rezek, J., et al. (2017). Metabolism of ibuprofen in higher plants: A model Arabidopsis thaliana cell suspension culture system. Environmental Pollution, 220, 383–392. https://doi.org/10.1016/j.envpol.2016.09.074.
Nuel, M., Laurent, J., Bois, P., Heintz, D., & Wanko, A. (2018). Seasonal and ageing effect on the behaviour of 86 drugs in a full-scale surface treatment wetland: Removal efficiencies and distribution in plants and sediments. Science of the Total Environment, 615, 1099–1109. https://doi.org/10.1016/j.scitotenv.2017.10.061.
Pelander, A., Tyrkkö, E., & Ojanperä, I. (2009). In silico methods for predicting metabolism and mass fragmentation applied to quietapine in liquid chromatography/time-of-flight mass spectrometry during drug screening. Rapid Communications in Mass Spectrometry, 23, 506–514. https://doi.org/10.1002/rcm.3901.
Rivas, D., Zonja, B., Eichhorn, P., Ginebreda, A., Pérez, S., & Barceló, D. (2017). Using MALDI-TOF MS imaging and LC-HRMS for the investigation of the degradation of polycaprolactone diol exposed to different wastewater treatments. Analytical and Bioanalytical Chemistry, 409(23), 5401–5411. https://doi.org/10.1007/s00216-017-0371-1.
Sandermann, H. (1999). Plant metabolism of organic xenobiotics. Status and prospects of the ‘Green Liver’ concept. In A. Altman, M. Ziv, & S. Izhar (Eds.), Plant biotechnology and in vitro biology in the 21st century (Vol. 36, pp. 321–328). Dordrecht: Springer. https://doi.org/10.1007/978-94-011-4661-6_74.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 Years of image analysis. Nature Methods, 9(7), 671–675. https://doi.org/10.1038/nmeth.2089.
Schymanski, E. L., Jeon, J., Gulde, R., Fenner, K., Ruff, M., Singer, H. P., et al. (2014). Identifying small molecules via high resolution mass spectrometry: Communicating confidence. Environmental Science and Technology, 48(4), 2097–2098. https://doi.org/10.1021/es5002105.
Sessitsch, A., Kuffner, M., Kidd, P., Vangronsveld, J., Wenzel, W. W., Fallmann, K., et al. (2013). The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biology & Biochemistry, 60, 182–194. https://doi.org/10.1016/j.soilbio.2013.01.012.
Thomas, F., & Cébron, A. (2016). Short-term rhizosphere effect on available carbon sources, phenanthrene degradation, and active microbiome in an aged-contaminated industrial soil. Frontiers in Microbiology, 7(February), 1–15. https://doi.org/10.3389/fmicb.2016.00092.
Urbaniak, M., Wyrwicka, A., Tołoczko, W., Serwecińska, L., & Zieliński, M. (2017). The effect of sewage sludge application on soil properties and willow (Salix sp.) cultivation. Science of the Total Environment, 586, 66–75. https://doi.org/10.1016/j.scitotenv.2017.02.012.
Van Eerd, L. L., Hoagland, R. E., Zablotowicz, R. M., & Hall, J. C. (2003). Pesticide metabolism in plants and microorganisms: An overview. Weed Science, 51, 472–495. https://doi.org/10.1021/bk-2001-0777.ch001.
Verbruggen, N., Hermans, C., & Schat, H. (2009). Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist, 181, 759–776.
Villette, C., Maurer, L., Delecolle, J., Zumsteg, J., Erhardt, M., & Heintz, D. (2019). In situ localization of micropollutants and associated stress response in Populus nigra leaves. Environment International, 126(March), 523–532. https://doi.org/10.1016/j.envint.2019.02.066.
Villette, C., Zumsteg, J., Schaller, H., & Heintz, D. (2018). Non-targeted metabolic profiling of BW312 Hordeum vulgare semi dwarf mutant using UHPLC coupled to QTOF high resolution mass spectrometry. Scientific Reports. https://doi.org/10.1038/s41598-018-31593-1.
Wani, B., Khan, A., & Bodha, R. (2011). Salix: A viable option for phytoremediation. African Journal of Environmental Science and Technology, 5(8), 567–571. https://doi.org/10.4314/ajest.v5i8.72048.
Zeilinger, S., Gupta, V. K., Dahms, T. E. S., Silva, R. N., Singh, H. B., Upadhyay, R. S., et al. (2016). Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiology Reviews, 40(2), 182–207. https://doi.org/10.1093/femsre/fuv045.
Zhang, D., Gersberg, R. M., Ng, W. J., & Tan, S. K. (2014). Removal of pharmaceuticals and personal care products in aquatic plant-based systems: A review. Environmental Pollution, 184, 620–639. https://doi.org/10.1016/j.envpol.2013.09.009.
Acknowledgements
We acknowledge the Agence de l’Eau Rhin Meuse (AERM) and the village of Falkwiller for access to the wetland. We thank Dr. Charles Pineau and his collaborators for sharing their knowledge on the MSI workflow.
Author information
Authors and Affiliations
Contributions
CV prepared the plant samples, conducted the LC-Q-TOF and MSI data acquisition, analyzed MSI data, prepared the figures and wrote the manuscript. LM performed water and sludge sample preparation and data analysis, prepared the figures and discussed the manuscript. AW revised the manuscript. DH contributed to the design of the experiments and sample preparation, discussed the results and revised the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare they have no conflict of interest with respect to this work.
Ethical approval
This article does not contain any studies with human and/or animal participants performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
11306_2019_1572_MOESM1_ESM.xlsx
Dataset S1: Full annotations obtained from water, sludge and leaf samples analyzed by LC–MS and predicted metabolites annotated in MSI datasets. Supplementary material 1 (XLSX 1449 kb)
Rights and permissions
About this article
Cite this article
Villette, C., Maurer, L., Wanko, A. et al. Xenobiotics metabolization in Salix alba leaves uncovered by mass spectrometry imaging. Metabolomics 15, 122 (2019). https://doi.org/10.1007/s11306-019-1572-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11306-019-1572-8