[en] Microcystin-LR (MC-LR) is a hepatotoxic metabolite that naturally occurs during some cyanobacterial blooms in eutrophic waterbodies, and irrigation of edible plants with MC-LR-contaminated water causes bioaccumulation of the toxin. However, sufficient information about accumulation and depuration mechanics in hydroculture-grown herb plants is still lacking. This work aimed at 1) investigating bioaccumulation and depuration of MC-LR in basil, 2) verifying the possible MC-LR detoxification mechanisms in the plant, and 3) detecting the natural occurrence of MC-LR in basil (n = 50) collected from the Belgian market. Basil plants grown in a hydroculture were exposed to MC-LR (5, 20, and 50 μg L-1) spiked in a Hoagland solution for seven days. MC-LR depuration was also studied by transferring the plants to a non-contaminated Hoagland solution after exposure to MC-LR for another seven days. MC-LR concentrations in Hoagland solution, basil leaves, and roots were quantified using a validated UHPLC-MS/MS method. In addition, ELISA and LC-HRMS (only basil leaves) were used for confirmation. The results showed an increase in the accumulated levels of MC-LR at higher exposure doses, with higher MC-LR levels in roots than in leaves for all the treatment conditions. For MC-LR depuration, significant reductions were observed in all the treatment conditions for roots only. No MC-LR conjugates, potentially related to metabolism, were detected by LC-HRMS. Finally, MC-LR was detected in one store-bought basil sample, representing the first occurrence of cyanotoxins in an edible crop from Belgium.
Disciplines :
Food science Environmental sciences & ecology
Author, co-author :
Van Hassel, Wannes ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
Abdallah, Mohamed F ; Department of Food Technology, Safety and Health, Faculty of Bioscience Engineering, Ghent University, Gent, 9000, Belgium, Department of Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Assiut University, Assiut, 71515, Egypt
Gracia Guzman Velasquez, Maria; Department of Food Technology, Safety and Health, Faculty of Bioscience Engineering, Ghent University, Gent, 9000, Belgium, Sciensano, Chemical and Physical Health Risks, Organic Contaminants and Additives, Leuvensesteenweg 17, Tervuren, 3080, Belgium
Miles, Christopher O ; Biotoxin Metrology, National Research Council Canada, Halifax, NS, B3H 3Z1, Canada, Norwegian Veterinary Institute, Postboks 64, 1431, Ås, Norway
H2020 - 965173 - Imptox - AN INNOVATIVE ANALYTICAL PLATFORM TO INVESTIGATE THE EFFECT AND TOXICITY OF MICRO AND NANO PLASTICS COMBINED WITH ENVIRONMENTAL CONTAMINANTS ON THE RISK OF ALLERGIC DISEASE IN PRECLINICAL AND CLINICAL
Funders :
EU - European Union UGent - Ghent University FPS Health Federal Public Service Health, Food Chain Safety and Environment
Funding text :
This work received funding from the Cyantir project, funded by the Federal Public Service (Health, Food Chain Safety and Environment), and the EU IMPTOX project (grant agreement No 965173).The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:Wannes Hugo R. Van Hassel reports financial support was provided by Federal Public Service Health Food Chain Safety and Environment. Mohamed F. Abdallah reports financial support was provided by Ghent university special research fund. Andreja Rajkovic reports financial support was provided by EU Framework Programme for Research and Innovation Euratom. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.Wannes Hugo R. Van Hassel received a full PhD scholarship within the Cyantir project. Mohamed F. Abdallah received a postdoctoral mandate from the Ghent University Special Research Fund (BOF), grant number BOF 01P03220. The ULC/BCCM provided the Microcystis ULC642 strain used to produce the MCs mixture (https://bccm.belspo.be/about-us/bccm-ulc).This work received funding from the Cyantir project, funded by the Federal Public Service (Health, Food Chain Safety and Environment), and the EU IMPTOX project (grant agreement No 965173 ).Wannes Hugo R. Van Hassel received a full PhD scholarship within the Cyantir project. Mohamed F. Abdallah received a postdoctoral mandate from the Ghent University Special Research Fund (BOF) , grant number BOF 01P03220 . The ULC/BCCM provided the Microcystis ULC642 strain used to produce the MCs mixture ( https://bccm.belspo.be/about-us/bccm-ulc ).
Abdallah, M.F., Van Hassel, W.H.R., Andjelkovic, M., Wilmotte, A., Rajkovic, A., Cyanotoxins and food contamination in developing countries: review of their types, toxicity, analysis, occurrence and mitigation strategies. Toxins, 13, 2021, 786, 10.3390/toxins13110786.
Bittencourt-Oliveira, M. do C., Cordeiro-Araújo, M.K., Chia, M.A., Arruda-Neto, J.D. de T., Oliveira, Ê.T., de Santos, F. dos, Lettuce irrigated with contaminated water: photosynthetic effects, antioxidative response and bioaccumulation of microcystin congeners. Ecotoxicol. Environ. Saf. 128 (2016), 83–90, 10.1016/j.ecoenv.2016.02.014.
Cao, Q., Liu, W., Jiang, W., Shu, X., Xie, L., Glutathione biosynthesis plays an important role in microcystin-LR depuration in lettuce and spinach. Environ. Pollut. 253 (2019), 599–605, 10.1016/j.envpol.2019.07.064.
Centre for the Promotion of Imports from developing countries, (CBI). The European Market Potential for Fresh Herbs. 2020 https://www.cbi.eu/market-information/fresh-fruit-vegetables/fresh-herbs/market-potential. (Accessed 1 February 2024)
Chen, J., Han, F.X., Wang, F., Zhang, H., Shi, Z., Accumulation and phytotoxicity of microcystin-LR in rice (Oryza sativa). Ecotoxicol. Environ. Saf. 76 (2012), 193–199, 10.1016/j.ecoenv.2011.09.022.
Chen, J., Song, L., Dai, J., Gan, N., Liu, Z., Effects of microcystins on the growth and the activity of superoxide dismutase and peroxidase of rape (Brassica napus L.) and rice (Oryza sativa L.). Toxicon 43 (2004), 393–400, 10.1016/J.TOXICON.2004.01.011.
Codd, G.A., Metcalf, J.S., Beattie, K.A., Retention of Microcystis aeruginosa and microcystin by salad lettuce (Lactuca sativa) after spray irrigation with water containing cyanobacteria. Toxicon 37 (1999), 1181–1185, 10.1016/S0041-0101(98)00244-X.
Corbel, S., Bouaïcha, N., Nélieu, S., Mougin, C., Soil irrigation with water and toxic cyanobacterial microcystins accelerates tomato development. Environ. Chem. Lett. 13 (2015), 447–452, 10.1007/s10311-015-0518-2.
Corbel, S., Mougin, C., Nélieu, S., Delarue, G., Bouaïcha, N., Evaluation of the transfer and the accumulation of microcystins in tomato (Solanum lycopersicum cultivar MicroTom) tissues using a cyanobacterial extract containing microcystins and the radiolabeled microcystin-LR (14C-MC-LR). Sci. Total Environ. 541 (2016), 1052–1058, 10.1016/j.scitotenv.2015.10.004.
Cordeiro-Araújo, M.K., Chia, M.A., Arruda-Neto, J.D. de T., Tornisielo, V.L., Vilca, F.Z., Bittencourt-Oliveira, M. do C., Microcystin-LR bioaccumulation and depuration kinetics in lettuce and arugula: human health risk assessment. Sci. Total Environ. 566–567 (2016), 1379–1386, 10.1016/j.scitotenv.2016.05.204.
Cordeiro-Araújo, M.K., Chia, M.A., Bittencourt-Oliveira, M. do C., Potential human health risk assessment of cylindrospermopsin accumulation and depuration in lettuce and arugula. Harmful Algae 68 (2017), 217–223, 10.1016/j.hal.2017.08.010.
Crush, J.R., Briggs, L.R., Sprosen, J.M., Nichols, S.N., Effect of irrigation with lake water containing microcystins on microcystin content and growth of ryegrass, clover, rape, and lettuce. Environ. Toxicol. 23 (2008), 246–252, 10.1002/tox.20331.
Freitas, M., Azevedo, J., Pinto, E., Neves, J., Campos, A., Vasconcelos, V., Effects of microcystin-LR, cylindrospermopsin and a microcystin-LR/cylindrospermopsin mixture on growth, oxidative stress and mineral content in lettuce plants (Lactuca sativa L.). Ecotoxicol. Environ. Saf. 116 (2015), 59–67, 10.1016/j.ecoenv.2015.02.002.
Hereman, T.C., Bittencourt-Oliveira, M. do C., Bioaccumulation of microcystins in lettuce. J. Phycol. 48 (2012), 1535–1537, 10.1111/jpy.12006.
Hoagland, D.R., Arnon, D.I., The water-culture method for growing plants without soil. Circ - Calif Agric Exp Stn 347 (1950), 1–32.
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. IARC monographs on the evaluation of carcinogenic risks to humans. Ingested nitrate and nitrite, and cyanobacterial peptide toxins. IARC Monogr. Eval. Carcinog. Risks Hum., 94, 2010, v –vii, 1–412.
Ibelings, B.W., Backer, L.C., Kardinaal, W.E.A., Chorus, I., Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae 40 (2014), 63–74, 10.1016/j.hal.2014.10.002.
Levizou, E., Papadimitriou, T., Papavasileiou, E., Papadimitriou, N., Kormas, K.A., Root vegetables bioaccumulate microcystins-LR in a developmental stage-dependent manner under realistic exposure scenario: the case of carrot and radish. Agric. Water Manag., 240, 2020, 106274, 10.1016/J.AGWAT.2020.106274.
Levizou, E., Statiris, G., Papadimitriou, T., Laspidou, C.S., Kormas, K.A., Lettuce facing microcystins-rich irrigation water at different developmental stages: effects on plant performance and microcystins bioaccumulation. Ecotoxicol. Environ. Saf. 143 (2017), 193–200, 10.1016/J.ECOENV.2017.05.037.
Llana-Ruiz-Cabello, M., Jos, A., Cameán, A., Oliveira, F., Barreiro, A., MacHado, J., Azevedo, J., Pinto, E., Almeida, A., Campos, A., Vasconcelos, V., Freitas, M., Analysis of the use of cylindrospermopsin and/or microcystin-contaminated water in the growth, mineral content, and contamination of Spinacia oleracea and Lactuca sativa. Toxins, 11, 2019, 624, 10.3390/toxins11110624.
Machado, J., Campos, A., Vasconcelos, V., Freitas, M., Effects of microcystin-LR and cylindrospermopsin on plant-soil systems: a review of their relevance for agricultural plant quality and public health. Environ. Res., 2017, 10.1016/j.envres.2016.09.015.
McElhiney, J., Lawton, L.A., Leifert, C., Investigations into the inhibitory effects of microcystins on plant growth, and the toxicity of plant tissues following exposure. Toxicon 39 (2001), 1411–1420, 10.1016/S0041-0101(01)00100-3.
Mohamed, Z., Bakr, A., Campos, A., Vasconcelos, V., Nasr, S.A.M., Growth inhibition and microcystin accumulation in bush bean (Phaseolus vulgaris L.) plant irrigated with water containing toxic Chrooccocus minutus. Agric. Water Manag., 261, 2022, 107381, 10.1016/j.agwat.2021.107381.
Mohamed, Z.A., Al Shehri, A.M., Microcystins in groundwater wells and their accumulation in vegetable plants irrigated with contaminated waters in Saudi Arabia. J. Hazard Mater. 172 (2009), 310–315, 10.1016/j.jhazmat.2009.07.010.
O'Neil, J.M., Davis, T.W., Burford, M.A., Gobler, C.J., The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14 (2012), 313–334, 10.1016/j.hal.2011.10.027.
Peuthert, A., Chakrabarti, S., Pflugmacher, S., Uptake of microcystins-LR and -LF (cyanobacterial toxins) in seedlings of several important agricultural plant species and the correlation with cellular damage (lipid peroxidation). Environ. Toxicol. 22 (2007), 436–442, 10.1002/tox.20266.
Pflugmacher, S., Wiegand, C., Beattie, K.A., Krause, E., Steinberg, C.E.W., Codd, G.A., Uptake, effects, and metabolism of cyanobacterial toxins in the emergent reed plant Phragmites australis (CAV.) Trin. Ex Steud. Environ. Toxicol. Chem. 20 (2001), 846–852, 10.1002/etc.5620200421.
Redouane, E.M., Tazart, Z., Lahrouni, M., Mugani, R., Elgadi, S., Zine, H., Zerrifi, S.E.A., Haida, M., Martins, J.C., Campos, A., Oufdou, K., Vasconcelos, V., Oudra, B., Health risk assessment of lake water contaminated with microcystins for fruit crop irrigation and farm animal drinking. Environ. Sci. Pollut. Res. 30 (2023), 80234–80244, 10.1007/s11356-023-27914-1.
Romero-Oliva, C.S., Contardo-Jara, V., Block, T., Pflugmacher, S., Accumulation of microcystin congeners in different aquatic plants and crops—a case study from lake Amatitlán, Guatemala. Ecotoxicol. Environ. Saf. 102 (2014), 121–128, 10.1016/j.ecoenv.2014.01.031.
Saha, S., Monroe, A., Day, M.R., Growth, yield, plant quality and nutrition of basil (Ocimum basilicum L.) under soilless agricultural systems. Ann. Agric. Sci. 61 (2016), 181–186, 10.1016/j.aoas.2016.10.001.
Samdal, I.A., Ballot, A., Løvberg, K.E., Miles, C.O., Multihapten approach leading to a sensitive ELISA with broad cross-reactivity to microcystins and nodularin. Environ. Sci. Technol. 48 (2014), 8035–8043, 10.1021/es5012675.
Svirčev, Z., Lalić, D., Bojadžija Savić, G., Tokodi, N., Drobac Backović, D., Chen, L., Meriluoto, J., Codd, G.A., Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings. Arch. Toxicol., 2019, 10.1007/s00204-019-02524-4.
Trajkovska-Broach, A., Anka, |, Petkoska, T., Mediterranean herbs, spices, and medicinal plants—natural remedies and rich sources of bioactive compounds. JSFA Reports 3 (2023), 4–12, 10.1002/JSF2.96.
Tsoumalakou, E., Papadimitriou, T., Berillis, P., Kormas, K.A., Levizou, E., Spray irrigation with microcystins-rich water affects plant performance from the microscopic to the functional level and food safety of spinach (Spinacia oleracea L.). Sci. Total Environ., 789, 2021, 147948, 10.1016/J.SCITOTENV.2021.147948.
Van Hassel, W.H.R., Andjelkovic, M., Durieu, B., Marroquin, V.A., Masquelier, J., Huybrechts, B., Wilmotte, A., A summer of cyanobacterial blooms in Belgian waterbodies: microcystin quantification and molecular characterizations. Toxins, 14, 2022, 61, 10.3390/toxins14010061.
Van Hassel, W.H.R., Huybrechts, B., Masquelier, J., Wilmotte, A., Andjelkovic, M., Development, validation and application of a targeted LC–MS method for quantification of microcystins and nodularin: towards a better characterization of drinking water. Water, 14, 2022, 1195, 10.3390/w14081195.
Van Hassel, W.H.R., Masquelier, J., Andjelkovic, M., Rajkovic, A., Towards a better quantification of cyanotoxins in fruits and vegetables: validation and application of an UHPLC-MS/MS-based method on Belgian products. Separations, 9, 2022, 319, 10.3390/separations9100319.
Wijewickrama, M.M., Manage, P.M., Accumulation of microcystin-LR in grains of two rice varieties (Oryza sativa L.) and a leafy vegetable, Ipomoea aquatica. Toxins, 11, 2019, 10.3390/toxins11080432.
Willame, R., Jurczak, T., Iffly, J.F., Kull, T., Meriluoto, J., Hoffmann, L., Distribution of hepatotoxic cyanobacterial blooms in Belgium and Luxembourg. Hydrobiologia 551 (2005), 99–117, 10.1007/S10750-005-4453-2/METRICS.
World Health Organization. Cyanobacterial Toxins: Microcystins. Background Document for Development of WHO Guidelines for Drinking-Water Quality and Guidelines for Safe Recreational Water Environments. 2020, WHO, Geneva, Switzerland.
Xiang, L., Li, Y.W., Liu, B.L., Zhao, H.M., Li, H., Cai, Q.Y., Mo, C.H., Wong, M.H., Li, Q.X., High ecological and human health risks from microcystins in vegetable fields in southern China. Environ. Int., 133, 2019, 105142, 10.1016/j.envint.2019.105142.
Zhang, Y., Whalen, J.K., Sauvé, S., Phytotoxicity and bioconcentration of microcystins in agricultural plants: meta-analysis and risk assessment. Environ. Pollut., 272, 2021, 115966, 10.1016/j.envpol.2020.115966.