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Considering the pro-inflammatory potential of cyanobacterial bloom extracts, including the bloom-associated heterotrophic bacteria, a cumulative action of several cyano- bacterial compounds is very likely [ , , , , ]. For example, LPS may contribute to local GIT tissue inflammation and thereby facilitate the access of other toxic compounds, like MCs, to deeper tissues and distribution to other organs and targets of toxicity such as the liver [ ].
Nodularia spumigena is favored in slightly saline environments; therefore, besides MCs, NOD is a major concern in the Baltic Sea and other brackish habitats [ , ].
Few data are available on NOD toxicokinetics, but a similar uptake mechanism OATP and mode of action PP1 and PP2A inhibition to MCs are proposed and partly supported by experimental evidence in zebrafish and different hepatic cell lines [ 5 , , ]. Despite severely inhibiting activity of PPs, NOD in contrast to MCs does not bind covalently to these ubiquitous cytoplasmic enzymes [ ].
The cyanobacterial neurotoxins anatoxin-a, anatoxin-a S , and saxitoxin are fast acting compounds, leading to paralysis and eventually respiratory failure within minutes to few hours [ , ]. Due to the rapid onset and specificity of neurological symptoms induced by inhibiting the transfer of excitatory signals, gastrointestinal irritation is unlikely to be a primary effect of these toxins.
Nevertheless, exposure to complex cyanobacterial blooms encompasses a mixture of various cyanobacterial, bacterial, and even xenobiotic and anthropogenic compounds. These may modulate the toxic effects of single compounds and result in gastrointestinal symptoms. An overview of enterotoxic effects linked to cyanobacterial blooms is given in Table 4.
Except of the well-recognized cyanotoxins, there are many potentially harmful bioactive secondary metabolites poorly characterized.
Many of these metabolites, like the non-ribosomal peptides aeruginosins, anabaenopeptins, or cyanopeptolins, have protease inhibiting activities, the latter has been also shown to cause neurotoxic effects and alter pathways linked to DNA damage and repair Table 4 [ , , , , , ]. Another group of poorly characterized cyanobacterial secondary metabolites are cyclic lipopeptides. Representatives of this group are, for example, anabaenolysins and puwainaphycins that cause damage to eukaryotic cell membranes in GIT models and induce necrotic effects Table 4 [ , , ].
More explicit effects on the GIT are reported by Humpage et al. Even though no known toxin was detected in the aqueous extract, there may be the presence of a variety of hydrophilic compound contributing to the effects observed.
The toxicological implications of these activities remain to be elucidated and the characterization of novel putative toxins in an effect-directed screening approach along with the description of structural characteristics should be highly encouraged. Regardless of the unknown toxic potential, these substances may contribute to the severity of gastroenteritis upon cyanobacterial intoxication, for example, by facilitating enteric hemorrhage through interference with the blood coagulation cascade [ ].
While single-agent toxic effects are often reported for detoxifying organs like the liver or the kidneys in toxicological studies, the most prominent symptom of harmful algal bloom intoxication is enterocolitis, probably mediated by co-action of multiple virulence factors. Besides the occasionally high abundance of identified cyanobacterial toxins, like MCs, many of the secondary compounds produced by cyanobacteria and eventually released to the water are unidentified or poorly characterized concerning their toxicity Table 4 [ , , ].
Furthermore, bloom-associated bacteria may contribute to the adverse effects observed upon exposure to cyanobacterial blooms, especially gastrointestinal illness [ 44 , ]. Also the role of LPS originating from both cyanobacteria and eubacteria has to be critically reflected.
The controversies about pro- or anti-inflammatory activities of cyanobacterial LPS may be explained by the effects of bloom-associated bacterial LPS, potentially sensitizing GIT epithelia for the effects of other toxins. A similar effect was observed with the pore-forming lipopeptides anabaenolysins A and B, where a transient increase in cell membrane permeability facilitated nodularin uptake, lowering the effective concentration for nodularin toxicity [ ].
Cyanobacterial LPS activity on the mucosal innate immune system does not sufficiently explain the GIT symptoms observed upon acute oral exposure to cyanobacterial blooms. However, the total bloom LPS released during a bloom, including pro-inflammatory LPS from bloom-associated bacteria, may facilitate the penetration of gastrointestinal epithelia and thereby promote the uptake of other cyanobacterial toxins by macrophages or into the blood via the paracellular route as suggested for CYN [ , ].
Considering the described activity of MC-LR as a tumor promoter and the suspicion of CYN carcinogenicity, the mixture of substances with diverse biological activity could finally contribute to colorectal cancer incidents upon long-term exposure to low concentrations, e. Cyanobacterial blooms are occurring more frequently and with increasing severity due to global climate change and eutrophication of water bodies, endangering the recreational value of water bodies as well as the safety of drinking water supplies.
For cyanobacterial bloom management, the precautionary principle is proposed, which means that the bloom is considered hazardous until proven safe [ ]. Despite gastrointestinal symptoms being the most reported and widespread malaise upon oral exposure to cyanobacterial blooms, research mostly focuses on specific organ toxicity of isolated toxins, i.
However, gastrointestinal and immunomodulatory effects have not been addressed sufficiently yet, including data allowing for quantitative assessments of dose—response relationships for acute and chronic adverse outcomes in the GIT in response to individual components of water blooms or their complex mixtures.
Regarding cyanobacterial effects on the immune system, we need a thorough investigation of mechanistic effects. Currently, effects to the mucosal immune system are predominantly reported as morphologically altered lymphoid follicles and changes in spleen size or weight during in vivo studies, but the underlying mechanisms are not investigated or discussed any further [ , ].
The findings summarized in this review need to be elaborated on and verified in a human health relevant system, as most studies are done in fish.
Disturbances in the immunological equilibrium including prolonged inflammation may pave the way for other chronic conditions, including carcinogenesis [ ].
Furthermore, sensitive subpopulations like children and people with chronic gastrointestinal inflammations e. These groups suffer more often and from more severe enteritis, as their mucosal immune system is still under development or in a permanently inflamed state.
In addition, with regard to the carcinogenic and genotoxic potential of MCs and NODs, low-level chronic exposure may contribute to colon carcinoma in later years [ 13 , , , ]. In the naturally occurring complex mixture of cyanobacterial bloom material, multiple factors can contribute to the adverse effect observed on the GIT and the associated mucosal immune system, probably not attributable to a single toxin or agent.
Nevertheless, even isolated toxins are reported to adversely affect the small intestine MC-LR and CYN or the stomach CYN , highlighting the importance of further investigation of this relevant system. We summarize evidence of inflammatory processes linked to cyanobacterial bloom exposure that may have a significant impact on chronic diseases, such as cancer-especially as some cyanotoxins MCs exhibit carcinogenic properties that may be synergistically enhanced by chronic inflammation.
To address the data gaps, we call for more comparable monitoring data to allow statistical meta- analyses and conclusive correlation of cyanobacterial blooms and health outcomes for further risk assessment studies.
No further limits Access type, publication date, document type etc. Forty-four publications were not eligible on the basis of their abstracts and eighty two underwent further full-text assessment. Of these, 66 articles were included for review purposes. Titles classified as highly relevant i. This review elaborates and expands on five review articles identified as highly relevant [ 4 , 6 , 7 , 8 , 9 ]. Chorus I, Bartram J Toxic cyanobacteria in water: a guide to their public health consequences, monitoring, and management.
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