{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,10]],"date-time":"2026-01-10T21:30:30Z","timestamp":1768080630675,"version":"3.49.0"},"reference-count":95,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2021,8,16]],"date-time":"2021-08-16T00:00:00Z","timestamp":1629072000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["UIDB\/04423\/2020"],"award-info":[{"award-number":["UIDB\/04423\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Frequent toxic cyanoblooms in eutrophic freshwaters produce various cyanotoxins such as the monocyclic heptapeptides microcystins (MCs), known as deleterious compounds to plant growth and human health. Recently, MCs are a recurrent worldwide sanitary problem in irrigation waters and farmland soils due to their transfer and accumulation in the edible tissues of vegetable produce. In such cases, studies about the persistence and removal of MCs in soil are scarce and not fully investigated. In this study, we carried out a greenhouse trial on two crop species: faba bean (Vicia faba var. Alfia 321) and common wheat (Triticum aestivum var. Achtar) that were grown in sterile (microorganism-free soil) and non-sterile (microorganism-rich soil) soils and subjected to MC-induced stress at 100 \u00b5g equivalent MC-LR L\u22121. The experimentation aimed to assess the prominent role of native rhizospheric microbiota in mitigating the phytotoxic impact of MCs on plant growth and reducing their accumulation in both soils and plant tissues. Moreover, we attempted to evaluate the health risk related to the consumption of MC-polluted plants for humans and cattle by determining the estimated daily intake (EDI) and health risk quotient (RQ) of MCs in these plants. Biodegradation was liable to be the main removal pathway of the toxin in the soil; and therefore, bulk soil (unplanted soil), as well as rhizospheric soil (planted soil), were used in this experiment to evaluate the accumulation of MCs in the presence and absence of microorganisms (sterile and non-sterile soils). The data obtained in this study showed that MCs had no significant effects on growth indicators of faba bean and common wheat plants in non-sterile soil as compared to the control group. In contrast, plants grown in sterile soil showed a significant decrease in growth parameters as compared to the control. These results suggest that MCs were highly bioavailable to the plants, resulting in severe growth impairments in the absence of native rhizospheric microbiota. Likewise, MCs were more accumulated in sterile soil and more bioconcentrated in root and shoot tissues of plants grown within when compared to non-sterile soil. Thereby, the EDI of MCs in plants grown in sterile soil was more beyond the tolerable daily intake recommended for both humans and cattle. The risk level was more pronounced in plants from the sterile soil than those from the non-sterile one. These findings suggest that microbial activity, eventually MC-biodegradation, is a crucial bioremediation tool to remove and prevent MCs from entering the agricultural food chain.<\/jats:p>","DOI":"10.3390\/microorganisms9081747","type":"journal-article","created":{"date-parts":[[2021,8,16]],"date-time":"2021-08-16T21:27:45Z","timestamp":1629149265000},"page":"1747","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Role of Rhizospheric Microbiota as a Bioremediation Tool for the Protection of Soil-Plant Systems from Microcystins Phytotoxicity and Mitigating Toxin-Related Health Risk"],"prefix":"10.3390","volume":"9","author":[{"given":"El Mahdi","family":"Redouane","sequence":"first","affiliation":[{"name":"Water, Biodiversity and Climate Change Laboratory, Phycology, Biotechnology and Environmental Toxicology Research Unit, Faculty of Sciences Semlalia, Cadi Ayyad University, Av. Prince My Abdellah, P.O. Box 2390, 40000 Marrakech, Morocco"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9012-4012","authenticated-orcid":false,"given":"Richard","family":"Mugani","sequence":"additional","affiliation":[{"name":"Water, Biodiversity and Climate Change Laboratory, Phycology, Biotechnology and Environmental Toxicology Research Unit, Faculty of Sciences Semlalia, Cadi Ayyad University, Av. Prince My Abdellah, P.O. Box 2390, 40000 Marrakech, Morocco"}]},{"given":"Majida","family":"Lahrouni","sequence":"additional","affiliation":[{"name":"Water, Biodiversity and Climate Change Laboratory, Phycology, Biotechnology and Environmental Toxicology Research Unit, Faculty of Sciences Semlalia, Cadi Ayyad University, Av. Prince My Abdellah, P.O. Box 2390, 40000 Marrakech, Morocco"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2134-6169","authenticated-orcid":false,"given":"Jos\u00e9 Carlos","family":"Martins","sequence":"additional","affiliation":[{"name":"CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450-208 Porto, Portugal"}]},{"given":"Soukaina El Amrani","family":"Zerrifi","sequence":"additional","affiliation":[{"name":"Water, Biodiversity and Climate Change Laboratory, Phycology, Biotechnology and Environmental Toxicology Research Unit, Faculty of Sciences Semlalia, Cadi Ayyad University, Av. Prince My Abdellah, P.O. Box 2390, 40000 Marrakech, Morocco"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7201-2041","authenticated-orcid":false,"given":"Khalid","family":"Oufdou","sequence":"additional","affiliation":[{"name":"Laboratory of Microbial Biotechnologies, Agrosciences and Environment, Department of Biology, Faculty of Science Semlalia, Cadi Ayyad University, P.O. Box  2390, 40000 Marrakech, Morocco"}]},{"given":"Alexandre","family":"Campos","sequence":"additional","affiliation":[{"name":"CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450-208 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3585-2417","authenticated-orcid":false,"given":"Vitor","family":"Vasconcelos","sequence":"additional","affiliation":[{"name":"CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450-208 Porto, Portugal"},{"name":"Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6295-9637","authenticated-orcid":false,"given":"Brahim","family":"Oudra","sequence":"additional","affiliation":[{"name":"Water, Biodiversity and Climate Change Laboratory, Phycology, Biotechnology and Environmental Toxicology Research Unit, Faculty of Sciences Semlalia, Cadi Ayyad University, Av. Prince My Abdellah, P.O. Box 2390, 40000 Marrakech, Morocco"}]}],"member":"1968","published-online":{"date-parts":[[2021,8,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1016\/j.jhydrol.2018.12.030","article-title":"Stricter nutrient criteria are required to mitigate the impact of climate change on harmful cyanobacterial blooms","volume":"569","author":"Huo","year":"2019","journal-title":"J. Hydrol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Chorus, I., and Welker, M. (2021). Understanding the occurrence of cyanobacteria and cyanotoxins. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management, Taylor and Francis. [2nd ed.].","DOI":"10.1201\/9781003081449"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"101845","DOI":"10.1016\/j.hal.2020.101845","article-title":"Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human- and climatically-altered world","volume":"96","author":"Paerl","year":"2020","journal-title":"Harmful Algae"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1007\/s10750-016-2967-4","article-title":"Long-term nutrient trends and harmful cyanobacterial bloom potential in hypertrophic Lake Taihu, China","volume":"787","author":"Xu","year":"2017","journal-title":"Hydrobiologia"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"4359","DOI":"10.1007\/s10750-019-04087-y","article-title":"Mitigating eutrophication and toxic cyanobacterial blooms in large lakes: The evolution of a dual nutrient (N and P) reduction paradigm","volume":"847","author":"Paerl","year":"2020","journal-title":"Hydrobiologia"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1016\/j.toxicon.2018.07.010","article-title":"Exposure routes and health effects of microcystins on animals and humans: A mini-review","volume":"151","author":"Massey","year":"2018","journal-title":"Toxicon"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1016\/j.chemosphere.2019.03.008","article-title":"Mode of action and fate of microcystins in the complex soil-plant ecosystems","volume":"225","author":"Redouane","year":"2019","journal-title":"Chemosphere"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.jenvman.2018.01.077","article-title":"An overview of the accumulation of microcystins in aquatic ecosystems","volume":"213","author":"Pham","year":"2018","journal-title":"J. Environ. Manag."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1007\/s10661-008-0220-y","article-title":"Identification and quantification of microcystins from a Nostoc muscorum bloom occurring in Ouka\u00efmeden river (High-Atlas mountains of Marrakech, Morocco)","volume":"149","author":"Oudra","year":"2009","journal-title":"Environ. Monit. Assess."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Massey, I.Y., Wu, P., Wei, J., Luo, J., Ding, P., Wei, H., and Yang, F. (2020). A mini-review on detection methods of microcystins. Toxins, 12.","DOI":"10.3390\/toxins12100641"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1118","DOI":"10.1016\/j.bmc.2017.08.040","article-title":"Microcystins: Synthesis and structure\u2013activity relationship studies toward PP1 and PP2A","volume":"26","author":"Fontanillo","year":"2018","journal-title":"Bioorg. Med. Chem."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"127868","DOI":"10.1016\/j.chemosphere.2020.127868","article-title":"MCLR induces dysregulation of calcium homeostasis and endoplasmic reticulum stress resulting in apoptosis in Sertoli cells","volume":"263","author":"Zhao","year":"2021","journal-title":"Chemosphere"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1016\/0041-0101(95)00101-8","article-title":"Stability of microcystins from cyanobacteria-II. Effect of UV light on decomposition and isomerization","volume":"33","author":"Tsuji","year":"1995","journal-title":"Toxicon"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"83","DOI":"10.2216\/i0031-8884-35-6S-83.1","article-title":"Stability of microcystins from cyanobacteria\u2014III.* Effect of pH and temperature","volume":"35","author":"Harada","year":"1996","journal-title":"Phycologia"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1007\/s00128-009-9910-6","article-title":"Effects of temperature on the stability of microcystins in muscle of fish and its consequences for food safety","volume":"84","author":"Zhang","year":"2010","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.tox.2011.12.011","article-title":"Human and rat hepatocyte toxicity and protein phosphatase 1 and 2A inhibitory activity of naturally occurring desmethyl-microcystins and nodularins","volume":"293","author":"Ufelmann","year":"2012","journal-title":"Toxicology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/j.watres.2018.12.048","article-title":"Cyanobacterial peptides beyond microcystins\u2014A review on co-occurrence, toxicity, and challenges for risk assessment","volume":"151","author":"Janssen","year":"2019","journal-title":"Water Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/j.scitotenv.2017.03.285","article-title":"Current research scenario for microcystins biodegradation\u2014A review on fundamental knowledge, application prospects and challenges","volume":"595","author":"Li","year":"2017","journal-title":"Sci. Total Environ."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/j.jhazmat.2015.08.041","article-title":"A review of reproductive toxicity of microcystins","volume":"301","author":"Chen","year":"2016","journal-title":"J. Hazard. Mater."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"5735","DOI":"10.1016\/j.watres.2012.08.003","article-title":"Determination of rate constants and half-lives for the simultaneous biodegradation of several cyanobacterial metabolites in Australian source waters","volume":"46","author":"Ho","year":"2012","journal-title":"Water Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1670","DOI":"10.1080\/10807039.2013.854138","article-title":"Fate and Persistence of Particulate and Dissolved Microcystin-LA from Microcystis Blooms","volume":"20","author":"Zastepa","year":"2014","journal-title":"Hum. Ecol. Risk Assess."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"143815","DOI":"10.1016\/j.scitotenv.2020.143815","article-title":"Distribution of microcystins in environmental multimedia and their bioaccumulation characteristics in marine benthic organisms in the Geum River Estuary, South Korea","volume":"757","author":"Kim","year":"2021","journal-title":"Sci. Total Environ."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.jhazmat.2009.07.010","article-title":"Microcystins in groundwater wells and their accumulation in vegetable plants irrigated with contaminated waters in Saudi Arabia","volume":"172","author":"Mohamed","year":"2009","journal-title":"J. Hazard. Mater."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1016\/j.chemosphere.2013.01.051","article-title":"Dissolved microcystins in surface and ground waters in regions with high cancer incidence in the Huai River Basin of China","volume":"91","author":"Tian","year":"2013","journal-title":"Chemosphere"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"129781","DOI":"10.1016\/j.chemosphere.2021.129781","article-title":"Quantitative screening for cyanotoxins in soil and groundwater of agricultural watersheds in Quebec, Canada","volume":"274","author":"Zhang","year":"2021","journal-title":"Chemosphere"},{"key":"ref_26","unstructured":"WHO (2020). Background Document for Development of WHO Guidelines for Drinking-Water Quality and Guidelines for Safe Recreational Water Environments. Cyanobacterial Toxins: Microcystins, World Health Organization."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1016\/j.envpol.2006.02.023","article-title":"Sorption, degradation and mobility of microcystins in Chinese agriculture soils: Risk assessment for groundwater protection","volume":"144","author":"Chen","year":"2006","journal-title":"Environ. Pollut."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1016\/j.jenvman.2006.12.040","article-title":"A laboratory study on risk assessment of microcystin-RR in cropland","volume":"86","author":"Bibo","year":"2008","journal-title":"J. Environ. Manag."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.envpol.2018.04.067","article-title":"Bioaccumulation of microcystin congeners in soil-plant system and human health risk assessment: A field study from Lake Taihu region of China","volume":"240","author":"Cao","year":"2018","journal-title":"Environ. Pollut."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/j.foodres.2017.09.079","article-title":"Fresh produce and their soils accumulate cyanotoxins from irrigation water: Implications for public health and food security","volume":"102","author":"Lee","year":"2017","journal-title":"Food Res. Int."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"105142","DOI":"10.1016\/j.envint.2019.105142","article-title":"High ecological and human health risks from microcystins in vegetable fields in southern China","volume":"133","author":"Xiang","year":"2019","journal-title":"Environ. Int."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1007\/s00128-019-02597-y","article-title":"Nitrogen Metabolism in Acorus calamus L. Leaves Induced Changes in Response to Microcystin\u2013LR at Environmentally Relevant Concentrations","volume":"103","author":"Chen","year":"2019","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1007\/s10646-020-02196-2","article-title":"Chronic effects of microcystin-LR at environmental relevant concentrations on photosynthesis of Typha angustifolia Linn","volume":"29","author":"Chen","year":"2020","journal-title":"Ecotoxicology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"127157","DOI":"10.1016\/j.chemosphere.2020.127157","article-title":"Response of hormone in rice seedlings to irrigation contaminated with cyanobacterial extract containing microcystins","volume":"256","author":"Liang","year":"2020","journal-title":"Chemosphere"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2381","DOI":"10.1897\/05-615R.1","article-title":"Effects of cyanobacterial toxins and cyanobacterial cell-free crude extract on germination of alfalfa (Medicago sativa) and induction of oxidative stress","volume":"25","author":"Pflugmacher","year":"2006","journal-title":"Environ. Toxicol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.mrrev.2008.07.003","article-title":"Repair and tolerance of oxidative DNA damage in plants","volume":"681","author":"Ariza","year":"2009","journal-title":"Mutat. Res. Rev. Mutat. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1111\/tpj.13299","article-title":"Reactive oxygen species, abiotic stress and stress combination","volume":"90","author":"Choudhury","year":"2017","journal-title":"Plant. J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"110351","DOI":"10.1016\/j.ecoenv.2020.110351","article-title":"Responses of antioxidative enzymes and gene expression in Oryza sativa L and Cucumis sativus L seedlings to microcystins stress","volume":"193","author":"Gu","year":"2020","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.ecoenv.2018.03.030","article-title":"Effects of light, microorganisms, farming chemicals and water content on the degradation of microcystin-LR in agricultural soils","volume":"156","author":"Cao","year":"2018","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Xiang, L., Li, Y.W., Wang, Z.R., Liu, B.L., Zhao, H.M., Li, H., Cai, Q.Y., Mo, C.H., and Li, Q.X. (2020). Bioaccumulation and Phytotoxicity and Human Health Risk from Microcystin-LR under Various Treatments: A Pot Study. Toxins, 12.","DOI":"10.3390\/toxins12080523"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1007\/s10646-011-0826-7","article-title":"Cyanobacterial extracts containing microcystins affect the growth, nodulation process and nitrogen uptake of faba bean (Vicia faba L., Fabaceae)","volume":"21","author":"Lahrouni","year":"2012","journal-title":"Ecotoxicology"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.toxicon.2013.10.003","article-title":"Physiological and antioxidant responses of Medicago sativa-rhizobia symbiosis to cyanobacterial toxins (Microcystins) exposure","volume":"76","author":"Oufdou","year":"2013","journal-title":"Toxicon"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"10037","DOI":"10.1007\/s11356-016-6223-2","article-title":"Microcystin-tolerant Rhizobium protects plants and improves nitrogen assimilation in Vicia faba irrigated with microcystin-containing waters","volume":"23","author":"Lahrouni","year":"2016","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Redouane, E.M., Lahrouni, M., Martins, J.C., El Amrani Zerrifi, S., Benidire, L., Douma, M., Aziz, F., Oufdou, K., Mandi, L., and Campos, A. (2021). Protective Role of Native Rhizospheric Soil Microbiota Against the Exposure to Microcystins Introduced into Soil-Plant System via Contaminated Irrigation Water and Health Risk Assessment. Toxins, 13.","DOI":"10.3390\/toxins13020118"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1016\/S0041-0101(00)00258-0","article-title":"Morphological and toxicological variability of Prorocentrum lima clones isolated from four locations in the south-west Indian Ocean","volume":"39","author":"Turquet","year":"2001","journal-title":"Toxicon"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1016\/j.ecoenv.2009.12.015","article-title":"Effect of different microcystin profiles on toxin bioaccumulation in common carp (Cyprinus carpio) larvae via Artemia nauplii","volume":"73","author":"Saqrane","year":"2010","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Bavithra, G., Azevedo, J., Oliveira, F., Morais, J., Pinto, E., Ferreira, I., Vasconcelos, V., Campos, A., and Almeida, C.M.R. (2020). Assessment of ConstructedWetlands\u2019 Potential for the Removal of Cyanobacteria and Microcystins (MC-LR). Water, 12.","DOI":"10.3390\/w12010010"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/j.envpol.2005.11.030","article-title":"Optimization of an effective extraction procedure for the analysis of microcystins in soils and lake sediments","volume":"143","author":"Chen","year":"2006","journal-title":"Environ. Pollut."},{"key":"ref_49","first-page":"1379","article-title":"Microcystin-LR bioaccumulation and depuration kinetics in lettuce and arugula: Human health risk assessment","volume":"566","author":"Chia","year":"2016","journal-title":"Sci. Total Environ."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1016\/j.scitotenv.2017.12.164","article-title":"Phytotoxicity, bioaccumulation and potential risks of plant irrigations using cyanobloom-loading freshwater","volume":"624","author":"Jia","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_51","unstructured":"FAO (2021). New Food Balances, Food and Agriculture Organization of the United Nations."},{"key":"ref_52","unstructured":"WHO (2011). Cyanobacterial Toxins: Microcystin-LR. Guidelines for Drinking-Water Quality, World Health Organization."},{"key":"ref_53","unstructured":"ANZECC (2000). Water Quality Guidelines, Livestock Drinking Water Guidelines."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"5405","DOI":"10.1007\/s11356-013-1535-y","article-title":"Physiological and biochemical defense reactions of Vicia faba L.-Rhizobium symbiosis face to chronic exposure to cyanobacterial bloom extract containing microcystins","volume":"20","author":"Lahrouni","year":"2013","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1002\/tox.20266","article-title":"Uptake of Microcystins-LR and -LF (Cyanobacterial Toxins) in Seedlings of Several Important Agricultural Plant Species and the Correlation with Cellular Damage (Lipid Peroxidation)","volume":"22","author":"Peuthert","year":"2007","journal-title":"Environ. Toxicol. Int. J."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Llana-ruiz-cabello, M., Jos, A., Came\u00e1n, A., Oliveira, F., Barreiro, A., Machado, J., Azevedo, J., Pinto, E., Almeida, A., and Campos, A. (2019). 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.","DOI":"10.3390\/toxins11110624"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.agwat.2018.04.011","article-title":"Effect of irrigation with microcystins-contaminated water on growth and fruit quality of Cucumis sativus L. and the health risk","volume":"204","author":"Zhu","year":"2018","journal-title":"Agric. Water Manag."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1080\/03601230802062307","article-title":"Effects of cyanobacteria producing microcystins on seed germination and seedling growth of several agricultural plants","volume":"43","author":"Saqrane","year":"2008","journal-title":"J. Environ. Sci. Heal. Part. B Pestic. Food Contam. Agric. Wastes"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.ecoenv.2017.11.020","article-title":"Effect of microcystins on root growth, oxidative response, and exudation of rice (Oryza sativa)","volume":"149","author":"Cao","year":"2018","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.ecoenv.2011.09.022","article-title":"Accumulation and phytotoxicity of microcystin-LR in rice (Oryza sativa)","volume":"76","author":"Chen","year":"2012","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"15116","DOI":"10.1007\/s11356-017-9061-y","article-title":"Variation in Cd accumulation among radish cultivars and identification of low-Cd cultivars","volume":"24","author":"Dai","year":"2017","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1016\/j.scitotenv.2018.04.354","article-title":"Genotypic variation and mechanism in uptake and translocation of perfluorooctanoic acid (PFOA) in lettuce (Lactuca sativa L.) cultivars grown in PFOA-polluted soils","volume":"636","author":"Xiang","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_63","first-page":"2028","article-title":"Impact of cyanobacterial toxins (microcystins) on growth and root development of in vitro Vicia faba cultures","volume":"12","author":"Lahrouni","year":"2015","journal-title":"Int. J. Innov. Appl. Stud."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Malaissi, L., Vaccarini, C.A., Hern\u00e1ndez, M.P., Ruscitti, M., Arango, C., Busquets, F., Arambarri, A.M., Giannuzzi, L., Andrinolo, D., and Sedan, D. (2020). [D-Leu1]MC-LR and MC-LR: A Small\u2013Large Difference: Significantly Different Effects on Phaseolus vulgaris L. (Fabaceae) Growth and Phototropic Response after Single Contact during Imbibition with Each of These Microcystin Variants. Toxins, 12.","DOI":"10.3390\/toxins12090585"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Pappas, D., Panou, M., Adamakis, I.D.S., Gkelis, S., and Panteris, E. (2020). Beyond microcystins: Cyanobacterial extracts induce cytoskeletal alterations in rice root cells. Int. J. Mol. Sci., 21.","DOI":"10.20944\/preprints202011.0659.v1"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"786","DOI":"10.1016\/j.toxicon.2009.01.028","article-title":"Physiological changes in Triticum durum, Zea mays, Pisum sativum and Lens esculenta cultivars, caused by irrigation with water contaminated with microcystins: A laboratory experimental approach","volume":"53","author":"Saqrane","year":"2009","journal-title":"Toxicon"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"115208","DOI":"10.1016\/j.envpol.2020.115208","article-title":"Irrigation of radish (Raphanus sativus L.) with microcystin-enriched water holds low risk for plants and their associated rhizopheric and epiphytic microbiome","volume":"266","author":"Petrou","year":"2020","journal-title":"Environ. Pollut."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.chemosphere.2013.04.079","article-title":"Microcystin-LR-induced phytotoxicity in rice crown root is associated with the cross-talk between auxin and nitric oxide","volume":"93","author":"Chen","year":"2013","journal-title":"Chemosphere"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"4573","DOI":"10.1007\/s12665-014-3746-z","article-title":"Response and recovery of rice (Oryza sativa) seedlings to irrigation with microcystin-contaminated water","volume":"73","author":"Liang","year":"2015","journal-title":"Environ. Earth Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"13942","DOI":"10.1007\/s11356-020-11642-x","article-title":"Effect of microcystins at different rice growth stages on its yield, quality, and safety","volume":"28","author":"Liang","year":"2020","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.1016\/j.scitotenv.2015.10.004","article-title":"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)","volume":"541","author":"Corbel","year":"2016","journal-title":"Sci. Total Environ."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"106274","DOI":"10.1016\/j.agwat.2020.106274","article-title":"Root vegetables bioaccumulate microcystins-LR in a developmental stage-dependent manner under realistic exposure scenario: The case of carrot and radish","volume":"240","author":"Levizou","year":"2020","journal-title":"Agric. Water Manag."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.ecoenv.2016.02.014","article-title":"Lettuce irrigated with contaminated water: Photosynthetic effects, antioxidative response and bioaccumulation of microcystin congeners","volume":"128","author":"Chia","year":"2016","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10661-019-7725-4","article-title":"Assessment of microcystin contamination of Amaranthus hybridus, Brassica oleracea, and Lactuca sativa sold in markets: A case study of Zaria, Nigeria","volume":"191","author":"Chia","year":"2019","journal-title":"Environ. Monit. Assess."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"948","DOI":"10.1016\/j.envpol.2009.10.023","article-title":"Detection of free and covalently bound microcystins in animal tissues by liquid chromatography-tandem mass spectrometry","volume":"158","author":"Neffling","year":"2010","journal-title":"Environ. Pollut."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1002\/tox.20331","article-title":"Effect of irrigation with lake water containing microcystins on microcystin content and growth of ryegrass, clover, rape, and lettuce","volume":"23","author":"Crush","year":"2008","journal-title":"Environ. Toxicol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1847","DOI":"10.1016\/S0041-0101(01)00166-0","article-title":"Ingestion of toxic Microcystis aeruginosa by dairy cattle and the implications for microcystin contamination of milk","volume":"39","author":"Orr","year":"2001","journal-title":"Toxicon"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1016\/S0041-0101(03)00006-0","article-title":"Exposure of beef cattle to sub-clinical doses of Microcystis aeruginosa: Toxin bioaccumulation, physiological effects and human health risk assessment","volume":"41","author":"Orr","year":"2003","journal-title":"Toxicon"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.1016\/S0043-1354(00)00419-X","article-title":"The adsorption of cyanobacterial hepatotoxins from water onto soil during batch experiments","volume":"35","author":"Miller","year":"2001","journal-title":"Water Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.jhazmat.2012.03.031","article-title":"Effects of humic acid and suspended soils on adsorption and photo-degradation of microcystin-LR onto samples from Taiwan reservoirs and rivers","volume":"217","author":"Thirumavalavan","year":"2012","journal-title":"J. Hazard. Mater."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"339","DOI":"10.2166\/wh.2005.049","article-title":"The adsorption of cyanobacterial hepatoxins as a function of soil properties","volume":"3","author":"Miller","year":"2005","journal-title":"J. Water Health"},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Esterhuizen, M., Schmitner, N., and Pflugmacher, S. (2021). Bioavailability of microcystin-LR in two different soil types to the legume Alfalfa Medicago sativa L. Int. J. Environ. Sci. Technol., 1\u201310.","DOI":"10.1007\/s13762-021-03132-5"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.ibiod.2016.07.011","article-title":"Biodegradation mechanism of microcystin-LR by a novel isolate of Rhizobium sp. TH and the evolutionary origin of the mlrA gene","volume":"115","author":"Zhu","year":"2016","journal-title":"Int. Biodeterior. Biodegrad."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1007\/s10532-011-9484-y","article-title":"Microbial degradation of microcystin in Florida\u2019s freshwaters","volume":"23","author":"Ramani","year":"2012","journal-title":"Biodegradation"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.scitotenv.2015.08.127","article-title":"Microbiote shift in the Medicago sativa rhizosphere in response to cyanotoxins extract exposure","volume":"539","author":"Oufdou","year":"2016","journal-title":"Sci. Total Environ."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1563","DOI":"10.1099\/ijs.0.63599-0","article-title":"Paucibacter toxinivorans gen. nov., sp. nov., a bacterium that degrades cyclic cyanobacterial hepatotoxins microcystins and nodularin","volume":"55","author":"Rapala","year":"2005","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/j.ecoenv.2007.03.013","article-title":"Biodegradation of microcystins by aquatic Burkholderia sp. from a South Brazilian coastal lagoon","volume":"69","author":"Lemes","year":"2008","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1779","DOI":"10.1080\/09593330.2011.556148","article-title":"Microbial degradation of microcystin-LR by Ralstonia solanacearum","volume":"32","author":"Zhang","year":"2011","journal-title":"Environ. Technol."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Mou, X., Lu, X., Jacob, J., Sun, S., and Heath, R. (2013). Metagenomic Identification of Bacterioplankton Taxa and Pathways Involved in Microcystin Degradation in Lake Erie. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061890"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1007\/s00128-018-2468-4","article-title":"Isolation and Characterization of Microcystin-Degrading Bacteria from Lake Erie","volume":"101","author":"Krishnan","year":"2018","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"13370","DOI":"10.1021\/es3027902","article-title":"Soil-based treatments of mechanically collected cyanobacterial blooms from Lake Taihu: Efficiencies and potential risks","volume":"46","author":"Chen","year":"2012","journal-title":"Environ. Sci. Technol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/j.jhazmat.2015.01.015","article-title":"Evaluation of the potential of anoxic biodegradation of intracellular and dissolved microcystins in lake sediments","volume":"286","author":"Wu","year":"2015","journal-title":"J. Hazard. Mater."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"2054","DOI":"10.1016\/j.egypro.2012.01.312","article-title":"Biodegradation of microcystins by Bacillus sp. Strain EMB","volume":"16","author":"Hu","year":"2012","journal-title":"Energy Procedia"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1795","DOI":"10.1007\/s10811-018-1403-8","article-title":"Establishment of a new strategy against Microcystis bloom using newly isolated lytic and toxin-degrading bacteria","volume":"30","author":"Lee","year":"2018","journal-title":"J. Appl. Phycol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"6319","DOI":"10.1021\/es903761y","article-title":"Evaluating Adsorption and Biodegradation Mechanisms during the Removal of Microcystin-RR by Periphyton","volume":"44","author":"Wu","year":"2010","journal-title":"Environ. Sci. Technol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/8\/1747\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:47:02Z","timestamp":1760165222000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/8\/1747"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,16]]},"references-count":95,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2021,8]]}},"alternative-id":["microorganisms9081747"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9081747","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,16]]}}}