Microcystin Contamination and Toxicity: Implications for Agriculture and Public Health
Abstract
1. Introduction
2. Microcystins
3. Contamination
3.1. Surface Water
3.2. Groundwater
3.3. Soil
4. Input Pathways
4.1. Irrigation with Polluted Water
4.2. Application of Cyanobacterial Manure
4.3. Compost
5. Toxicity
5.1. Biosynthesis
5.2. Mechanism of Action
5.3. Ecotoxicity
5.4. Phytotoxicity
6. Agricultural Plants
6.1. Plant Seedling Growth
6.2. Tissue Growth
6.3. Aquatic Plants
Species | Environment | Mode of Uptake | * Microcystin Toxins | ** Concentration of Microcystin | *** Plant Response | Reference |
---|---|---|---|---|---|---|
Alternanthera philoxeroides (alligator weed) | Submerged | Root absorption Diffusion | Total MCs | 169–3945 ng/g | -- | [107] |
Ceratophyllum dermersum (hornwort) | Submerged | Root absorption Diffusion | MC-LR | 71 µg/g | -- | [103] |
Elodea canadensis (American waterweed) | Submerged | Root absorption Leaf contact with water surface Diffusion | MC-LR | 40 µg/g | -- | [103] |
Hydrilla verticillata (water thyme) | Submerged | Root absorption Diffusion | Total MCs MC-LR MC-RR MC-YR | >1000 µg/kg >1000 µg/kg <500 µg/kg <500 µg/kg | Biotransformation of MCs | [108] |
Lemna gibba (duckweed) | Floating | Root absorption Leaf contact with water surface | MC-LR | 2.44 µg/g | Reduction in plant growth and chlorophyll content Biotransformation of MCs | [109] |
Phragmites australis (common reed) | Floating | Root absorption Leaf contact with water surface | MC-LR | 5–40 µg/L | Inhibition of growth and development | [110] |
Polygonum portorcensis (smooth smartweed) | Submerged | Root absorption Diffusion | Total MCs MC-LR MC-RR MC-YR | >400 µg/kg >400 µg/kg <200 µg/kg <200 µg/kg | Biotransformation of MCs | [108] |
Trapa natans (water chestnut) | Floating | Root absorption Leaf contact with water surface | Total MCs | 1.68 ng/g | -- | [111] |
Typha sp. (cattail) | Floating | Root absorption Leaf contact with water surface | Total MCs MC-LR MC-RR MC-YR | >1500 µg/kg >1500 µg/kg <500 µg/kg <500 µg/kg | Biotransformation of MCs | [108] |
Vallisneria natans (eelgrass) | Submerged | Root absorption Diffusion | MC-RR | 10 mg/L | Reduction in root and leaf numbers | [105] |
7. Human Health Risks
8. Implications for Future Research
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Withers, P.J.A.; Neal, C.; Jarvie, H.P.; Doody, D.G. Agriculture and eutrophication: Where do we go from here? Sustainability 2014, 6, 5853–5875. [Google Scholar] [CrossRef]
- Rabalais, N.N.; Turner, R.E.; Díaz, R.J.; Justić, D. Global change and eutrophication of coastal waters. ICES J. Mar. Sci. 2009, 66, 1528–1537. [Google Scholar] [CrossRef]
- Duncan, E.; Kleinman, P.J.; Sharpley, A.N. Eutrophication of Lakes and Rivers; John Wiley & Sons: Chichester, UK, 2012. [Google Scholar]
- Padedda, B.M.; Sechi, N.; Lai, G.G.; Mariani, M.A.; Pulina, S.; Sarria, M.; Satta, C.T.; Virdis, T.; Buscarinu, P.; Lugliè, A. Consequences of eutrophication in the management of water resources in Mediterranean reservoirs: A case study of Lake Cedrino (Sardinia, Italy). Glob. Ecol. Conserv. 2017, 12, 21–35. [Google Scholar] [CrossRef]
- Neilan, B.A.; Pearson, L.A.; Muenchhoff, J.; Moffitt, M.C.; Dittmann, E. Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ. Microbiol. 2013, 15, 1239–1253. [Google Scholar] [CrossRef] [PubMed]
- Welker, M.; von Döhren, H. Cyanobacterial peptides—Nature’s own combinatorial biosynthesis. FEMS Microbiol. Rev. 2006, 30, 530–563. [Google Scholar] [CrossRef]
- Van Apeldoorn, M.E.; Van Egmond, H.P.; Speijers, G.J.A.; Bakker, G.J.I. Toxins of cyanobacteria. Mol. Nutr. Food Res. 2007, 51, 7–60. [Google Scholar] [CrossRef]
- Bailiu-Rodriguez, D.; Peraino, N.J.; Premathilaka, S.H.; Birbeck, J.A.; Baliu-Rodriguez, T.; Westrick, J.A.; Isailovic, D. Identification of novel microcystins using high-resolution MS and MSn with python code. Environ. Sci. Technol. 2022, 56, 1652–1663. [Google Scholar] [CrossRef]
- Cao, L.; Huang, F.; Massey, I.Y.; Wen, C.; Zheng, S.; Xu, S.; Yang, F. Effects of microcystin-LR on the microstructure and inflammation-related factors of jejunum in mice. Toxins 2019, 11, 482. [Google Scholar] [CrossRef]
- Catherine, A.; Bernard, C.; Spoof, L.; Bruno, M. Microcystins and Nodularins. In Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis; Meriluoto, J., Lisa Spoof, L., Codd, G.A., Eds.; John Wiley & Sons, Ltd.: Chichester, UK, 2017; pp. 107–126. [Google Scholar]
- Sivonen, K.; Jones, G. Cyanobacterial Toxins. In Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management; Chorus, I., Bartram, J., Eds.; E and FN Spon: London, UK, 1999; pp. 41–111. [Google Scholar]
- WHO. Cyanobacterial Toxins: Microcystins. In Guidelines for Drinking Water Quality and Guidelines for Safe Recreational Water Environments; World Health Organization: Geneva, Switzerland, 2020. [Google Scholar]
- Lad, A.; Breidenbach, J.D.; Su, R.C.; Murray, J.; Kuang, R.; Mascarenhas, A.; Najjar, J.; Patel, S.; Hegde, P.; Youssef, M.; et al. As we drink and breathe: Adverse health effects of microcystins and other harmful algal bloom toxins in the liver, gut, lungs and beyond. Toxins 2022, 12, 418. [Google Scholar] [CrossRef]
- Drobac, D.; Tokodi, N.; Simeunović, J.; Baltić, V.; Stanić, D.; Svirčev, Z. Human exposure to cyanotoxins and their effects on health. Arhiv za Higijenu Rada i Toksikologiju 2013, 64, 119–130. [Google Scholar] [CrossRef]
- Jochimsen, E.M.; Carmichael, W.W.; An, J.S.; Cardo, D.M.; Cookson, S.T.; Holmes, C.E.; Antunes, M.B.; de Melo Filho, D.A.; Lyra, T.M.; Barreto, V.S.; et al. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Eng. J. Med. 1998, 338, 873–878. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Xie, P.; Li, L.; Xu, J. First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicol. Sci. 2009, 108, 81–89. [Google Scholar] [CrossRef] [PubMed]
- Ueno, Y.; Nagata, S.; Tsutsumi, T.; Hasegawa, A.; Watanabe, M.F.; Park, H.D.; Chen, G.C.; Yu, S.Z. Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 1996, 17, 1317–1321. [Google Scholar] [CrossRef]
- Svirčev, Z.; Drobac, D.; Tokodi, N.; Lužanin, Z.; Munjas, A.M.; Nikolin, B.; Vuleta, D.; Meriluoto, J. Epidemiology of cancers in Serbia and possible connection with cyanobacterial blooms. J. Environ. Sci. Health Part C 2014, 32, 319–337. [Google Scholar] [CrossRef] [PubMed]
- MacKintosh, C.; Beattie, K.A.; Klumpp, S.; Cohen, P.; Codd, G.A. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett. 1990, 264, 187–192. [Google Scholar] [CrossRef]
- Dawson, R.M. The toxicology of microcystins. Toxicon 1998, 36, 953–962. [Google Scholar] [CrossRef]
- Greer, B.; Meneely, J.P.; Elliott, C.T. Uptake and accumulation of Microcystin-LR based on exposure through drinking water: An animal model assessing the human health risk. Sci. Rep. 2018, 8, 4913. [Google Scholar] [CrossRef]
- Fischer, W.J.; Altheimer, S.; Cattori, V.; Meier, P.J.; Dietrich, D.R.; Hagenbuch, B. Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin. Toxicol. Appl. Pharmacol. 2005, 203, 257–263. [Google Scholar] [CrossRef]
- Lezcano, N.; Sedán, D.; Lucotti, I.; Giannuzzi, L.; Vittone, L.; Andrinolo, D.; Mundiña-Weilenmann, C. Subchronic microcystin-LR exposure increased hepatic apoptosis and induced compensatory mechanisms in mice. J. Biochem. Mol. Toxicol. 2012, 26, 131–138. [Google Scholar] [CrossRef]
- Zhou, W.; Zhang, X.; Xie, P.; Liang, H.; Zhang, X. The suppression of hematopoiesis function in Balb/c mice induced by prolonged exposure of microcystin-LR. Toxicol. Lett. 2013, 219, 194–201. [Google Scholar] [CrossRef]
- Campos, A.; Redouane, E.M.; Freitas, M.; Amaral, S.; Azevedo, T.; Loss, L.; Máthé, C.; Mohamed, Z.A.; Oudra, B.; Vasconcelos, V. Impacts of microcystins on morphological and physiological parameters of agricultural plants: A review. Plants 2021, 10, 639. [Google Scholar] [CrossRef] [PubMed]
- Liang, C.; Wang, W. Response and recovery of rice (Oryza sativa) seedlings to irrigation with microcystin-contaminated water. Environ. Ear. Sci. 2015, 73, 4573–4580. [Google Scholar] [CrossRef]
- Zhang, Y.; Husk, B.R.; Dinh, Q.T.; Sanchez, J.S.; Sauvé, S.; Whalen, J.K. Quantitative screening for cyanotoxins in soil and groundwater of agricultural watersheds in Quebec, Canada. Chemosphere 2021, 274, 129781. [Google Scholar] [CrossRef]
- 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. 2019, 133, 105142. [Google Scholar] [CrossRef]
- de Figueiredo, D.R.; Azeiteiro, U.M.; Esteves, S.M.; Gonçalves, F.J.M.; Pereira, M.J. Microcystin-producing blooms—A serious global public health issue. Ecol. Environ. Saf. 2004, 59, 151–163. [Google Scholar] [CrossRef] [PubMed]
- 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. 2009, 172, 310–315. [Google Scholar] [CrossRef]
- Yang, Z.; Kong, F.; Zhang, M. Groundwater contamination by microcystin from toxic cyanobacteria blooms in Lake Chaohu, China. Environ. Monit. Assess. 2016, 188, 280. [Google Scholar] [CrossRef]
- Groundwater: Understanding and Protecting Our Hidden Resource; U.S. Environmental Protection Agency: Washington, DC, USA. Available online: https://www.epa.gov/sciencematters/groundwater-understanding-and-protecting-our-hidden-resource (accessed on 18 October 2021).
- Gobler, C.J.; Burkholder, J.M.; Davis, T.W.; Harke, M.J.; Johengen, T.; Stow, C.A.; Waal, D.B.V. The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 2016, 56, 87–97. [Google Scholar] [CrossRef]
- Pfister, S.; Bayer, P.; Koehler, A.; Hellweg, S. Environmental impacts of water use in global crop production: Hotspots and trade-offs with land use. Environ. Sci. Technol. 2011, 45, 13. [Google Scholar] [CrossRef]
- Mutoti, M.; Gumbo, J.; Jideani, A.I.O. Occurrence of cyanobacteria in water used for food production: A review. Phys. Chem. Earth. 2022, 125, 103101. [Google Scholar] [CrossRef]
- Bláha, L.; Babica, P.; Maršálek, B. Toxins produced in cyanobacterial water blooms—Toxicity and risks. Interdiscip. Toxicol. 2009, 2, 36–41. [Google Scholar] [CrossRef] [PubMed]
- Massey, I.Y.; Yang, F. A mini review on microcystins and bacterial degradation. Toxins 2020, 12, 268. [Google Scholar] [CrossRef]
- Schmidt, J.R.; Wilhelm, S.W.; Boyer, G.L. The fate of microcystins in the environment and challenges for monitoring. Toxins 2014, 6, 3354–3387. [Google Scholar] [CrossRef]
- Chorus, I.; Fastner, J.; Welker, M. Cyanobacteria and cyanotoxins in a changing environment: Concepts, controversies, challenges. Water 2021, 13, 2463. [Google Scholar] [CrossRef]
- Peng, L.; Liu, Y.; Chen, W.; Liu, L.; Kent, M.; Song, L. Health risks associated with consumption of microcystin-contaminated fish and shellfish in three Chinese lakes: Significance for freshwater aquacultures. Ecotoxicol. Environ. Saf. 2010, 73, 1804–1811. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Li, L.; Gan, N.; Zheng, L.; Ma, H.; Shan, K.; Liu, J.; Xiao, B.; Song, L. Seasonal dynamics of water bloom-forming Microcystis morphospecies and the associated extracellular microcystin concentrations in large, shallow, eutrophic Dianchi Lake. J. Environ. Sci. 2014, 26, 1921–1929. [Google Scholar] [CrossRef]
- Chen, W.T. Analysis on eutrophication and cyanobacteria blooms characteristics in Dashahe Reservoir. Guangdong Water Resour. Hydropower 2015, 6, 33–35. [Google Scholar]
- Harada, K.; Tsuji, K.; Watanabe, M.F.; Kondo, F. Stability of microcystins from cyanobacteria—III. Effect of pH and temperature. Phycologia 1996, 35, 83–88. [Google Scholar] [CrossRef]
- Tsuji, K.; Naito, S.; Kondo, F.; Ishikawa, N.; Watanabe, M.F.; Suzuki, M.; Harada, K. Stability of microcystins from cyanobacteria: Effect of light on decomposition and isomerization. Environ. Sci. Technol. 1994, 28, 173–177. [Google Scholar] [CrossRef]
- Rastogi, R.P.; Sinha, R.P.; Incharoensakdi, A. The cyanotoxin-microcystins: Current overview. Rev. Environ. Sci. Biol. Technol. 2014, 13, 215–249. [Google Scholar] [CrossRef]
- Chen, W.; Song, L.; Gan, N.; Li, L. Sorption, degradation and mobility of microcystins in Chinese agriculture soils: Risk assessment for groundwater protection. Environ Pollut. 2006, 144, 752–758. [Google Scholar] [CrossRef]
- Wen, H.F. Toxicological effects of microcystin-LR on earthworm (Eisenia fetida) in soil. Biol. Fertil. Soils 2017, 53, 849–860. [Google Scholar] [CrossRef]
- Ding, Q.; Liu, K.; Song, Z.; Sun, R.; Zhang, J.; Yin, L.; Pu, Y. Effects of microcystin-LR on metabolic functions and structure succession of sediment bacterial community under anaerobic conditions. Toxins 2020, 12, 183. [Google Scholar] [CrossRef] [PubMed]
- Corbel, S.; Mougin, C.; Nélieu, S.; Delarue, G.; Bouaïcha, N. Evaluation of the transfer and the accumulation of microcystins in tomato (Solanum lycopersicum cultivar Micro Tom) tissues using a cyanobacterial extract containing microcystins and the radiolabeled microcystin-LR (14 C-MC-LR). Sci. Total Environ. 2016, 541, 1052–1058. [Google Scholar] [CrossRef] [PubMed]
- Cao, Q.; Steinman, A.D.; Wan, X.; Xie, L. Bioaccumulation of microcystin congeners in soil-plant system and human health risk assessment: A field study from Lake Taihu region of China. Environ. Pollut. 2018, 240, 44–50. [Google Scholar] [CrossRef] [PubMed]
- Esterhuizen-Londt, M.; Pfugmacher, S. Vegetables cultivated with exposure to pure and naturally occurring β-N-methylaminol-alanine (BMAA) via irrigation. Environ. Res. 2019, 169, 357–361. [Google Scholar] [CrossRef] [PubMed]
- 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. 2007, 22, 436–442. [Google Scholar] [CrossRef]
- 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. 2008, 23, 246–252. [Google Scholar] [CrossRef]
- Singh, J.S.; Kumar, A.; Rai, A.N.; Singh, D.P. Cyanobacteria: A precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front. Microbiol. 2016, 7, 529. [Google Scholar] [CrossRef]
- Chittora, D.; Meena, M.; Barupal, T.; Swapnil, P. Cyanobacteria as a source of biofertilizers for sustainable agriculture. Biochem. Biophys. Rep. 2020, 12, 100737. [Google Scholar] [CrossRef]
- Xiang, L.; Li, Y.W.; Wang, Z.R.; Liu, B.L.; Zhao, H.M.; Li, H.; Cai, Q.Y.; Mo, C.H.; Li, Q.X. Bioaccumulation and phytotoxicity and human health risk from microcystin-LR under various treatments: A pot study. Toxins 2020, 12, 523. [Google Scholar] [CrossRef]
- Falconer, I.R. Tumor promotion and liver-injury caused by oral consumption of cyanobacteria. Environ. Toxicol. Water Qual. 1991, 6, 177–184. [Google Scholar] [CrossRef]
- Sinha, R.; Soni, B.K.; Agarwal, S.M.; Shankar, B.; Hahn, G.E. Vermiculture for organic horticulture: Producing chemical-free, nutritive and health protective foods by earthworms. Agric. Sci. 2013, 17–44. [Google Scholar] [CrossRef]
- Li, Y.; Wang, Y.; Yin, L.; Pu, Y.; Wang, D. Using the nematode Caenorhabditis elegans as a model animal for assessing the toxicity induced by microcystin-LR. J. Environ. Sci. 2009, 21, 395–401. [Google Scholar]
- Cao, Q.; Steinman, A.D.; Yao, L.; Xie, L. Effects of light, microorganisms, farming chemicals and water content on the degradation of microcystin-LR in agricultural soils. Ecotoxicol. Environ. Saf. 2018, 156, 141–147. [Google Scholar] [CrossRef] [PubMed]
- Gurtler, J.B.; Doyle, M.P.; Erickson, M.C.; Jiang, X.; Millner, P.; Sharma, M. Composting to inactivate foodborne pathogens for crop soil application: A review. J. Food. Prot. 2018, 1821–1837. [Google Scholar] [CrossRef]
- 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, 153, 191–204. [Google Scholar] [CrossRef]
- Mikalsen, B.; Bojson, G.; Skulberg, O.M.; Fastner, J.; Davies, W.; Gabrielsen, T.M.; Rudi, K.; Jakobsen, K.S. Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J. Bacteriol. 2003, 185, 2774–2785. [Google Scholar] [CrossRef] [PubMed]
- Felnagle, E.A.; Jackson, E.E.; Chan, Y.A.; Podevels, A.M.; Berti, A.D.; McMahon, M.D.; Thomas, M.G. Nonribosomal peptide synthetases involved in the production of medically relevant natural products. Mol. Pharm. 2008, 5, 191–211. [Google Scholar] [CrossRef]
- Bouaïcha, N. Cyanobacterial toxins: Modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 2014, 96, 1–15. [Google Scholar]
- Fontanillo, M.; Köhn, M. Microcystins: Synthesis and structure–activity relationship studies toward PP1 and PP2A. Bioorg. Med. Chem. 2018, 26, 1118–1126. [Google Scholar] [CrossRef]
- Craig, M.; Luu, H.A.; McCready, T.L.; Williams, D.; Andersen, R.J.; Holmes, C.F. Molecular mechanisms underlying he interaction of motuporin and microcystins with type-1 and type-2A protein phosphatases. Biochem. Cell Biol. 1996, 74, 569–578. [Google Scholar] [CrossRef] [PubMed]
- Ferrão-Filho, A.D.S.; Kozlowsky-Suzuki, B. Cyanotoxins: Bioaccumulation and effects on aquatic animals. Mar. Drugs 2011, 9, 2729–2772. [Google Scholar] [CrossRef]
- Carmichael, W.W.; Boyer, G.L. Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes. Harmful Algae 2016, 54, 194–212. [Google Scholar] [CrossRef]
- Toivola, D.M.; Omary, M.B.; Ku, N.O.; Peltola, O.; Baribault, H.; Eriksson, J.E. Protein phosphatase inhibition in normal and keratin 8/18 assembly-incompetent mouse strains supports a functional role of keratin intermediate filaments in preserving hepatocyte integrity. Hepatology 1998, 28, 116–128. [Google Scholar] [CrossRef] [PubMed]
- Frangež, R.; Žužek, M.C.; Mrkun, J.; Šuput, D.; Sedmak, B.; Kosek, M. Microcystin-LR affects cytoskeleton and morphology of rabbit primary whole embryo cultured cells in vitro. Toxicon 2003, 41, 999–1005. [Google Scholar] [CrossRef]
- Pappas, D.; Gkelis, S.; Panteris, E. The effects of microcystin-LR in Oryza sativa root cells: F-actin as a new target of cyanobacterial toxicity. Plant Biol. 2020, 22, 839–849. [Google Scholar] [CrossRef] [PubMed]
- Abe, T.; Lawson, T.; Weyers, J.D.B.; Codd, G.A. Microcystin-LR inhibits photosynthesis of Phaseolus vulgaris primary leaves: Implications for current spray irrigation practice. New Phytol. 1996, 133, 651–658. [Google Scholar] [CrossRef]
- 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. 2021, 789, 147948. [Google Scholar] [CrossRef]
- Wang, N.; Wang, C. Effects of microcystin-LR on the tissue growth and physiological responses of the aquatic plant Iris pseudacorus L. Aquat. Toxicol. 2018, 200, 197–205. [Google Scholar] [CrossRef]
- Chen, G.; Li, Q.; Bai, M.; Chen, Y. Nitrogen metabolism in Acorus calamus L. leaves induced changes in response to microcystin-LR at environmentally relevant concentrations. Bull. Environ. Contam. Toxicol. 2019, 103, 280–285. [Google Scholar] [CrossRef]
- Llana-Ruiz-Cabello, M.; Jos, A.; Cameán, A.; Oliveira, F.; Barreiro, A.; Machado, J.; Azevedo, J.; Pinto, E.; Almeida, A.; Campos, A.; et al. 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 2019, 11, 624. [Google Scholar] [CrossRef]
- 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. 2015, 116, 59–67. [Google Scholar] [CrossRef]
- Zhang, Y.; Whalen, J.K.; Sauvé, S. Phytotoxicity and bioconcentration of microcystins in agricultural plants: Meta-analysis and risk assessment. Environ. Pollut. 2020, 272, 115966. [Google Scholar] [CrossRef]
- Zhao, W.; Fu, P.; Liu, G.; Zhao, P. Difference between emergent aquatic and terrestrial monocotyledonous herbs in relation to the coordination of leaf stomata with vein traits. AoB PLANTS 2020, 12, plaa047. [Google Scholar] [CrossRef]
- 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 2004, 15, 393–400. [Google Scholar] [CrossRef]
- Machado, J.; Azevedo, J.; Freitas, M.; Pinto, E.; Almeida, A.; Vasconcelos, V.; Campos, A. Analysis of the use of microcystin-contaminated water in the growth and nutritional quality of the root-vegetable, Daucus carota. Environ. Sci. Pollut. Res. 2017, 24, 752–764. [Google Scholar] [CrossRef]
- Gehringer, M.M.; Kewada, V.; Coates, N.; Downing, T.G. The use of Lepidium sativum in a plant bioassay system for the detection of microcystin-LR. Toxicon 2003, 41, 871–876. [Google Scholar] [CrossRef]
- Pflugmacher, S.; Jung, K.; Lundvall, L.; Neumann, S.; Peuthert, A. Effects of cyanobacterial toxins and cyanobacterial cell-free crude extract on germination of alfalfa (Medicago sativa) and induction of oxidative stress. Environ. Toxicol. Chem 2006, 25, 381–2387. [Google Scholar] [CrossRef]
- Cao, Q.; Rediske, R.R.; Yao, L.; Xie, L. Effect of microcystins on root growth, oxidative response, and exudation of rice (Oryza sativa). Ecotoxicol. Environ. Saf. 2018, 149, 143–149. [Google Scholar] [CrossRef] [PubMed]
- Malaissi, L.; Vaccarini, C.A.; Hernández, M.P.; Ruscitti, M.; Arango, C.; Busquets, F.; Arambarri, A.M.; Giannuzzi, L.; Andrinolo, D.; Sedan, D. [D-Leu1] MC-LR and MC-LR: A small–large 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 2020, 12, 585. [Google Scholar] [CrossRef]
- Corbel, S.; Bouaïcha, N.; Nélieu, S.; Mougin, C. Soil irrigation with water and toxic cyanobacterial microcystins accelerates tomato development. Environ. Chem. Lett. 2015, 13, 447–452. [Google Scholar] [CrossRef]
- Pflugmacher, S.; Hofmann, J.; Hübner, B. Effects on growth and physiological parameters in wheat (Triticum aestivum L.) grown in soil and irrigated with cyanobacterial toxin contaminated water. Environ. Toxicol. Chem. 2007, 26, 2710–2716. [Google Scholar] [CrossRef]
- El-Sheekh, M.M.; Khairy, H.M.; El-Shenody, R. Effects of crude extract of Microcystis aeruginosa on germination, growth and chlorophyll content of Zea mays L. Bangladesh J. Bot. 2013, 42, 295–300. [Google Scholar]
- Järvenpää, S.; Lundberg-Niinistö, C.; Sjövall, O.; Tyystjärvi, E.; Meriluoto, J. Effects of microcystins on broccoli and mustard, and analysis of accumulated toxin by liquid chromatography-mass spectrometry. Toxicon 2007, 49, 865–874. [Google Scholar] [CrossRef]
- Hereman, T.C.; Bittencourt-Olveira, M.C. Bioaccumulation of microcystins in lettuce. J. Phycol. 2012, 48, 1535–1537. [Google Scholar] [CrossRef]
- Lahrouni, M.; Oufdou, K.; El Khalloufi, F.; Benidire, L.; Albert, S.; Göttfert, M.; Caviedes, M.A.; Rodriguez-Llorente, I.D.; Oudra, B.; Pajuelo, E. Microcystin-tolerant Rhizobium protects plants and improves nitrogen assimilation in Vicia faba irrigated with microcystin-containing waters. Environ. Sci. Pollut. Res. Int. 2016, 23, 10037–10049. [Google Scholar] [CrossRef]
- Bittencourt-Olveira, M.C.; Cordeiro-Araújo, M.K.; Chia, M.A.; Arrudo-Neto, J.D.; de Oliveira, E.T.; dos Santos, F. Lettuce irrigated with contaminated water: Photosynthetic effects, antioxidative response and bioaccumulation of microcystin congeners. Ecotoxicol. Environ. Safi. 2016, 128, 83–90. [Google Scholar] [CrossRef]
- Haida, M.; El Khalloufi, F.; Mugani, R.; Redouane, E.M.; Campos, A.; Vasconcelos, V.; Oudra, B. Effects of irrigation with microcystin-containing water on growth, physiology, and antioxidant defense in strawberry Fragaria vulgaris under hydroponic culture. Toxins 2022, 14, 198. [Google Scholar] [CrossRef]
- Lee, S.; Jiang, X.; Manubolu, M.; Riedl, K.; Ludsin, S.A.; Martin, J.F.; Lee, J. Fresh produce and their soils accumulate cyanotoxins from irrigation water: Implications for public health and food security. Food Res. Int. 2017, 102, 234–245. [Google Scholar] [CrossRef]
- Pflugmacher, S.; Aulhorn, M.; Grimm, B. Influence of a cyanobacterial crude extract containing microcystin-LR on the physiology and antioxidative defence systems of different spinach variants. New Phytol. 2007, 175, 482–489. [Google Scholar] [CrossRef] [PubMed]
- Lucini, L.; Bernardo, L. Comparison of proteome response to saline and zinc in lettuce. Front. Plant Sci. 2015, 16, 240. [Google Scholar] [CrossRef] [PubMed]
- 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. Exotoxicol. Environ. Saf. 2017, 143, 193–200. [Google Scholar] [CrossRef]
- Pereira, S.; Saker, M.L.; Vale, M.; Vasconcelos, V.M. Comparison of sensitivity of grasses (Lolium perenne L. and Festuca rubra L.) and lettuce (Lactuca sativa L.) exposed to water contaminated with microcystins. Bull. Environ. Contam. Toxicol. 2009, 83, 81–84. [Google Scholar] [CrossRef]
- Gutiérrez-Praena, D.; Campos, A.; Azevedo, J.; Neves, J.; Freitas, M.; Guzmán-Guillén, R.; Cameán, A.M.; Renaut, J.; Vasconcelos, V. Exposure of Lycopersicon esculentum to microcystin-LR: Effects in the leaf proteome and toxin translocation from water to leaves and fruits. Toxins 2014, 6, 1837–1854. [Google Scholar] [CrossRef] [PubMed]
- Cao, Q.; Wan, X.; Shu, X.; Xie, L. Bioaccumulation and detoxifixation of microcystin-LR in three submerged macrophytes: The important role of glutathione biosynthesis. Chemosphere 2019, 225, 935–942. [Google Scholar] [CrossRef]
- Mitrovic, S.M.; Allis, O.; Furey, A.; James, K.J. Bioaccumulation and harmful effects of microcystin-LR in the aquatic plants Lemna minor and Wolffia arrhiza and the filamentous alga Chladophora fracta. Ecotoxicol. Environ. Saf. 2005, 61, 345–352. [Google Scholar] [CrossRef]
- Pflugmacher, S.; Wiegand, C.; Beattie, K.A.; Codd, G.A.; Steinberg, C.E.W. Uptake of the cyanobacterial hepatotoxin microcystin-LR by aquatic macrophytes. Appl. Bot. 1998, 72, 228–232. [Google Scholar]
- Cao, Q.; Liu, W.; Jiang, W.; Shu, X.; Xie, L. Glutathione biosynthesis plays an important role in microcystin-LR depurination in lettuce and spinach. Environ. Pollut. 2019, 253, 599–605. [Google Scholar] [CrossRef]
- Yin, L.; Huang, J.; Li, D.; Liu, Y. Microcystin-RR uptake and its effects on the growth of submerged macrophyte Vallisneria natans (lour.) hara. Environ. Toxicol. 2005, 20, 308–313. [Google Scholar] [CrossRef]
- Wang, Z.; Xiao, B.; Song, L.; Wang, C.; Zhang, J. Responses and toxin bioaccumulation in duckweed (Lemna minor) under microcystin-LR, linear alkybenzene sulfonate and their joint stress. J. Hazard Mater. 2012, 229–230, 137–144. [Google Scholar] [CrossRef]
- Song, L.; Chen, W.; Peng, L.; Wan, N.; Gan, N.; Zhang, X. Distribution and bioaccumulation of microcystins in water columns: A systematic investigation into the environmental fate and the risks associated with microcystins in Meilang Bay, Lake Taihu. Water Res. 2007, 41, 2853–2864. [Google Scholar] [CrossRef] [PubMed]
- Romero-Oliva, C.S.; Contardo-Jara, V.; Pflugmacher, S. Time dependent uptake, bioaccumulation and biotransformation of cell free crude extract microcystins from Lake Amatitlán, Guatemala by Ceratophyllum demersum, Egeria densa and Hydrilla verticillata. Toxicon 2015, 105, 62–73. [Google Scholar] [CrossRef]
- Saqrane, S.; Ghazali, I.E.; Ouahid, Y.; Hassni, M.E.; Hadrami, I.E.; Bouarab, L.; del Campo, F.F.; Oudra, B.; Vasconcelos, V. Phytotoxic effects of cyanobacteria extract on the aquatic plant Lemna gibba: Microcystin accumulation, detoxication and oxidative stress induction. Aquat. Toxicol. 2007, 83, 284–294. [Google Scholar] [CrossRef]
- Máthé, C.; M-Hamvas, M.; Vasas, G.; Surányi, G.; Bácsi, I.; Beyer, D.; Tóth, S.; Tímár, M.; Borbély, G. Microcystin-LR, a cyanobacterial toxin, induces growth inhibition and histological alterations in common reed (Phragmites australis) plants regenerated from embryogenic calli. New Phytol. 2007, 176, 824–835. [Google Scholar] [CrossRef]
- Xiao, F.G.; Zhao, X.L.; Tang, J.; Gu, X.H.; Zhang, J.P.; Niu, W.M. Necessity of screening water chestnuts for microcystins after cyanobacterial blooms break out. Arch. Environ. Contam. Toxicol. 2009, 57, 256–263. [Google Scholar] [CrossRef]
- Melaram, R. Environmental risk factors implicated in liver disease: A mini-review. Front. Public Health 2021, 9, 683719. [Google Scholar] [CrossRef]
Species | Experimental Design | Concentration of Microcystin * | Duration of Exposure (Days) | Stage of Development | Physiological Effects | Reference |
---|---|---|---|---|---|---|
Brassica juncea (mustard green) | Pot study | 150 µg/kg MC-LR | 10 d | Mature plants | Reduced plant height and weight | [56] |
Brassica napus (rape seed) | Germination | 600–3000 µg/L MC-LR | 10 d | Seeds | Reduced germination | [81] |
Daucus carota (carrot) | Independent exposure experiment | 50 µg/L MC-LR | 28 d | Mature plants | Reduced root growth Increased photosynthetic efficiency | [82] |
Ipomoea batatas (sweet potato) | Pot study | 150 µg/kg MC-LR | 10 d | Mature plants | Reduced plant height and weight | [56] |
Lactuca sativa (lettuce) | Hydroponics Hydroponics | 50 µg/L MCs 100 µg/L MC-LR | 21 d 10 d | Mature plants Mature plants | Reduced leaf growth and mineral content Reduced biomass of leaves and mineral content Increased GST activity in roots | [77,78] |
Lepidium sativum (watercress) | Germination | 10 µg/L MC-LR | 6 d | Seeds | Reduced radicle length and shoot weight | [83] |
Medicago sativa (alfalfa) | Germination | 5 µg/L MCs | 7 d | Seedlings | Inhibition of germination and root growth Increased lipid peroxidation | [84] |
Oryza sativa (rice) | Hydroponics Hydroponics | 1–3000 µg/L MC 500 µg/L MCs | 7 d 30 d | Seedlings | Reduced biomass of leaves, stems, and roots Reduced root weight, length, surface area and volume Increased levels of tartaric acid and malic acid | [26] [85] |
Phaseolus vulgaris (green bean) | Germination | 3500 µg/L MC-LR | 30 d | Seeds | Reduced chlorophyll content, delayed development Reduced conductivity and phototropic response | [86] |
Solanium lycopersicum (tomato) | Soil | 5 µg/L MC-LR | 90 d | Seeds | Stimulation of inflorescence and blooming of flower | [87] |
Spinacia oleracea (spinach) | Hydroponics | 50 µg/L MCs | 21 d | Mature plants | Reduced leaf growth and mineral content | [77] |
Triticum aestivum (wheat) | Germination Soil | 0.5 µg/L MC-LR | 3 d 14 d | Seeds | Reduced germination Reduced photosynthesis and root and shoot development Increased GST activity | [88] |
Zea mays (corn) | Germination | 100,000–800,000 µg/L | 1 d | Seeds | Reduced plant height and weight | [89] |
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Melaram, R.; Newton, A.R.; Chafin, J. Microcystin Contamination and Toxicity: Implications for Agriculture and Public Health. Toxins 2022, 14, 350. https://doi.org/10.3390/toxins14050350
Melaram R, Newton AR, Chafin J. Microcystin Contamination and Toxicity: Implications for Agriculture and Public Health. Toxins. 2022; 14(5):350. https://doi.org/10.3390/toxins14050350
Chicago/Turabian StyleMelaram, Rajesh, Amanda R. Newton, and Jennifer Chafin. 2022. "Microcystin Contamination and Toxicity: Implications for Agriculture and Public Health" Toxins 14, no. 5: 350. https://doi.org/10.3390/toxins14050350
APA StyleMelaram, R., Newton, A. R., & Chafin, J. (2022). Microcystin Contamination and Toxicity: Implications for Agriculture and Public Health. Toxins, 14(5), 350. https://doi.org/10.3390/toxins14050350