Health risk assessment of lake water contaminated with microcystins for fruit crop irrigation and farm animal drinking

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Abstract

The health risks linked to the consumption of microcystin-accumulating crops have been increasing worldwide in toxic cyanobloom-occurring regions. The bioaccumulation of microcystins (MCs) in agricultural produce at environmentally realistic concentrations is poorly investigated. In this field study, we assessed the health risks of MCs in raw water used for irrigating fruit crops (bioaccumulation) and watering farm animals in the Lalla Takerkoust agricultural region (Marrakesh, Morocco). Thus, MCs were extracted from water and fruit samples and quantified by enzyme-linked immunosorbent assay in order to calculate the health risk indicators. MCs posed a high health-risk level to poultry and horses, with estimated daily intakes (EDI) being 14- and 19-fold higher than the recommended limits (3.1 and 2.3 μg MC-LR L ⁻¹), respectively. Furthermore, pomegranate posed the same level of risk, with EDI being 22- and 53-fold higher than the limit dose (0.04 μg MC-LR kg ⁻¹) for adults and children, respectively. There was an urgent need for guidelines regarding water use and management in MC-polluted areas, besides the setup of nature-based tools for toxin removal from raw water used in farming practices. Moreover, MCs could contaminate the human food chain, which implies further investigations of their potential accumulation in livestock- and poultry-based food.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11356-023-27914-1.

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Most cited references 58

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A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp.

Matthew J. Harke, Morgan Steffen, Christopher Gobler … (2016)

This review summarizes the present state of knowledge regarding the toxic, bloom-forming cyanobacterium, Microcystis, with a specific focus on its geographic distribution, toxins, genomics, phylogeny, and ecology. A global analysis found documentation suggesting geographic expansion of Microcystis, with recorded blooms in at least 108 countries, 79 of which have also reported the hepatatoxin microcystin. The production of microcystins (originally "Fast-Death Factor") by Microcystis and factors that control synthesis of this toxin are reviewed, as well as the putative ecophysiological roles of this metabolite. Molecular biological analyses have provided significant insight into the ecology and physiology of Microcystis, as well as revealed the highly dynamic, and potentially unstable, nature of its genome. A genetic sequence analysis of 27 Microcystis species, including 15 complete/draft genomes are presented. Using the strictest biological definition of what constitutes a bacterial species, these analyses indicate that all Microcystis species warrant placement into the same species complex since the average nucleotide identity values were above 95%, 16S rRNA nucleotide identity scores exceeded 99%, and DNA-DNA hybridization was consistently greater than 70%. The review further provides evidence from around the globe for the key role that both nitrogen and phosphorus play in controlling Microcystis bloom dynamics, and the effect of elevated temperature on bloom intensification. Finally, highlighted is the ability of Microcystis assemblages to minimize their mortality losses by resisting grazing by zooplankton and bivalves, as well as viral lysis, and discuss factors facilitating assemblage resilience.

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State of knowledge and concerns on cyanobacterial blooms and cyanotoxins.

Shane Snyder, Estelle Baurès, Q Walker … (2013)

Cyanobacteria are ubiquitous microorganisms considered as important contributors to the formation of Earth's atmosphere and nitrogen fixation. However, they are also frequently associated with toxic blooms. Indeed, the wide range of hepatotoxins, neurotoxins and dermatotoxins synthesized by these bacteria is a growing environmental and public health concern. This paper provides a state of the art on the occurrence and management of harmful cyanobacterial blooms in surface and drinking water, including economic impacts and research needs. Cyanobacterial blooms usually occur according to a combination of environmental factors e.g., nutrient concentration, water temperature, light intensity, salinity, water movement, stagnation and residence time, as well as several other variables. These environmental variables, in turn, have promoted the evolution and biosynthesis of strain-specific, gene-controlled metabolites (cyanotoxins) that are often harmful to aquatic and terrestrial life, including humans. Cyanotoxins are primarily produced intracellularly during the exponential growth phase. Release of toxins into water can occur during cell death or senescence but can also be due to evolutionary-derived or environmentally-mediated circumstances such as allelopathy or relatively sudden nutrient limitation. Consequently, when cyanobacterial blooms occur in drinking water resources, treatment has to remove both cyanobacteria (avoiding cell lysis and subsequent toxin release) and aqueous cyanotoxins previously released. Cells are usually removed with limited lysis by physical processes such as clarification or membrane filtration. However, aqueous toxins are usually removed by both physical retention, through adsorption on activated carbon or reverse osmosis, and chemical oxidation, through ozonation or chlorination. While the efficient oxidation of the more common cyanotoxins (microcystin, cylindrospermopsin, anatoxin and saxitoxin) has been extensively reported, the chemical and toxicological characterization of their by-products requires further investigation. In addition, future research should also investigate the removal of poorly considered cyanotoxins (β-methylamino-alanine, lyngbyatoxin or aplysiatoxin) as well as the economic impact of blooms. © 2013 Elsevier Ltd. All rights reserved.

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Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice.

Nidhi Gupta, S.C. Pant, R. Vijayaraghavan … (2003)

The cyclic peptide toxins microcystins and nodularins are the most common and abundant cyanotoxins present in diverse water systems. They have been the cause of human and animal health hazards and even death. Over 60 microcystin variants have been reported so far. We report here the results of our study on comparative toxicity evaluation of three most predominant microcystins, MC-LR, MC-RR and MC-YR in mice. The mice were administered one LD(50) dose of MC-LR, RR and YR (43, 235.4 and 110.6 micro g/kg body weight, respectively), and biochemical and histological variables were determined at 30 min post-treatment and mean time to death (MTD). Significant increase in liver body weight index was induced by all three variants. There was marginal increase in serum levels of hepatic enzymes viz. AST, ALT and gamma-GT at 30 min post-treatment but 3-4 fold increase was observed at MTD. In contrast, enhanced LDH leakage, DNA fragmentation and depletion of hepatic glutathione was observed at 30 min post treatment in all three variants. There was no change in levels of serum protein, albumin and albumin/globulin ratio. Liver histology showed time dependent severe pathological lesions like congestion, haemorrhage, portal mononuclear cell infiltration and obliteration of chromatin material. Lung lesions were predominantly in bronchi and parenchyma. Though qualitatively lesions were identical in all three microcystin variants, degree of liver and lung lesions varied quantitatively with the toxin. The breathing pattern and respiratory frequency of the mice after i.p. administration of the toxin showed uniform pattern for 90 min followed by abrupt change in the respiratory pattern and instantaneous death. Based on biochemical and histological studies, MC-LR was found to be the most potent toxin followed by MC-YR and MC-RR.

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Author and article information

Contributors

Vitor Vasconcelos:

ORCID: http://orcid.org/0000-0003-3585-2417

vmvascon@fc.up.pt

Journal

Journal ID (nlm-ta): Environ Sci Pollut Res Int

Journal ID (iso-abbrev): Environ Sci Pollut Res Int

Title: Environmental Science and Pollution Research International

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0944-1344

ISSN (Electronic): 1614-7499

Publication date (Electronic): 9 June 2023

Publication date PMC-release: 9 June 2023

Publication date (Print): 2023

Volume: 30

Issue: 33

Pages: 80234-80244

Affiliations

[1 ]GRID grid.411840.8, ISNI 0000 0001 0664 9298, Water, Biodiversity and Climate Change Laboratory, Faculty of Sciences Semlalia, , Cadi Ayyad University, ; 40000 Marrakech, Morocco

[2 ]GRID grid.5808.5, ISNI 0000 0001 1503 7226, CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, ; Terminal de Cruzeiros do Porto de Leixões, 4450-208 Matosinhos, Portugal

[3 ]GRID grid.411840.8, ISNI 0000 0001 0664 9298, Laboratory of Microbial Biotechnologies, Agrosciences, and Environment (BioMAgE), Labeled Research Unit-CNRST N°4, Faculty of Sciences Semlalia, , Cadi Ayyad University, ; 40000 Marrakech, Morocco

[4 ]GRID grid.424661.3, ISNI 0000 0001 2173 3068, Laboratory of Agro. Food Technology and Quality, Regional Center for Agronomic Research of Marrakech, , National Institute of Agronomic Research (INRA), ; 40000 Marrakech, Morocco

[5 ]Geology and Sustainable Mining Institute (GSMI), Mohammad VI Polytechnic University, 43150 Ben Guerir, Morocco

[6 ]Higher Institute of Nurses Professions and Health Techniques of Guelmim, 81000 Guelmim, Morocco

[7 ]GRID grid.5808.5, ISNI 0000 0001 1503 7226, Department of Biology, Faculty of Sciences, , University of Porto, ; 4169-007 Porto, Portugal

Author notes

Responsible Editor: Philippe Garrigues

Author information

Vitor Vasconcelos http://orcid.org/0000-0003-3585-2417

Article

Publisher ID: 27914

DOI: 10.1007/s11356-023-27914-1

PMC ID: 10344998

PubMed ID: 37294489

SO-VID: d44a71fd-0cde-40d8-9b31-1d32cb54b8f7

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 16 February 2023

Date accepted : 21 May 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100010661, Horizon 2020 Framework Programme;

Award ID: 823860

Award Recipient : El Mahdi Redouane

Funded by: Universidade do Porto

Open Access :

Open access funding provided by FCT|FCCN (b-on).

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ScienceOpen disciplines: General environmental science

Keywords: microcystins,raw water,farm animals,fruit crops,bioaccumulation,health risk

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ScienceOpen disciplines: General environmental science

Keywords: microcystins, raw water, farm animals, fruit crops, bioaccumulation, health risk

Health risk assessment of lake water contaminated with microcystins for fruit crop irrigation and farm animal drinking

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Abstract

Supplementary Information

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Hydrology

Most cited references 58

A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp.

State of knowledge and concerns on cyanobacterial blooms and cyanotoxins.

Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice.

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Author notes

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