Environmental conditions that influence toxin biosynthesis in cyanobacteria.
TL;DR: This review focuses on the environmental regulation of some of the most relevant cyanotoxin, namely the microcystins, nodularin, cylindrospermopsin, saxitoxins, anatoxins and jamaicamides.
Abstract: Over the past 15 years, the genetic basis for production of many cyanobacterial bioactive compounds has been described This knowledge has enabled investigations into the environmental factors that regulate the production of these toxins at the molecular level Such molecular or systems level studies are also likely to reveal the physiological role of the toxin and contribute to effective water resource management This review focuses on the environmental regulation of some of the most relevant cyanotoxins, namely the microcystins, nodularin, cylindrospermopsin, saxitoxins, anatoxins and jamaicamides
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TL;DR: In this article, the applicability and feasibility of various controls and management approaches for natural waters and drinking water supplies are discussed, and a key underlying approach that should be considered in almost all instances is nutrient (both N and P) input reductions; which have been shown to effectively reduce cyanobacterial biomass, and therefore limit health risks and frequencies of hypoxic events.
Abstract: Cyanobacteria are the Earth’s oldest oxygenic photoautotrophs and have had major impacts on shaping its biosphere. Their long evolutionary history (∼3.5 by) has enabled them to adapt to geochemical and climatic changes, and more recently anthropogenic modifications of aquatic environments, including nutrient over-enrichment (eutrophication), water diversions, withdrawals, and salinization. Many cyanobacterial genera exhibit optimal growth rates and bloom potentials at relatively high water temperatures; hence global warming plays a key role in their expansion and persistence. Bloom-forming cyanobacterial taxa can be harmful from environmental, organismal, and human health perspectives by outcompeting beneficial phytoplankton, depleting oxygen upon bloom senescence, and producing a variety of toxic secondary metabolites (e.g., cyanotoxins). How environmental factors impact cyanotoxin production is the subject of ongoing research, but nutrient (N, P and trace metals) supply rates, light, temperature, oxidative stressors, interactions with other biota (bacteria, viruses and animal grazers), and most likely, the combined effects of these factors are all involved. Accordingly, strategies aimed at controlling and mitigating harmful blooms have focused on manipulating these dynamic factors. The applicability and feasibility of various controls and management approaches is discussed for natural waters and drinking water supplies. Strategies based on physical, chemical, and biological manipulations of specific factors show promise; however, a key underlying approach that should be considered in almost all instances is nutrient (both N and P) input reductions; which have been shown to effectively reduce cyanobacterial biomass, and therefore limit health risks and frequencies of hypoxic events.
1,162 citations
Cites background from "Environmental conditions that influ..."
...The cues for toxin synthesis are likely subject to multiple environmental and cellular factors acting in unresolved synergistic or antagonistic combinations [55, 86, 176]....
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TL;DR: 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 are highlighted.
704 citations
Cites background from "Environmental conditions that influ..."
...hypotheses that nitrogen and possibly iron may influence microcystin synthesis (Martin-Luna et al., 2006; Ginn et al., 2010; Neilan et al., 2013)....
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...…sequence motifs for both the DNA binding proteins Fur (ferric uptake regulator) and ntcA (global nitrogen regulator): observations that support the hypotheses that nitrogen and possibly iron may influence microcystin synthesis (Martin-Luna et al., 2006; Ginn et al., 2010; Neilan et al., 2013)....
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TL;DR: Relationships between NH4+ and NO3− metabolism have important implications for harmful algal blooms, development of nutrient criteria for management, and modeling of nutrient uptake by phytoplankton, particularly in conditions where eutrophication is increasing and the redox state of N loads is changing.
Abstract: Anthropogenic activities are altering total nutrient loads to many estuaries and freshwaters, resulting in high loads not only of total nitrogen (N), but in some cases, of chemically reduced forms, notably NH4+. Long thought to be the preferred form of N for phytoplankton uptake, NH4+ may actually suppress overall growth when concentrations are sufficiently high. NH4+ has been well known to be inhibitory or repressive for NO3‐ uptake and assimilation, but the concentrations of NH4+ that promote vs. repress NO3‐ uptake, assimilation, and growth in different phytoplankton groups and under different growth conditions are not well understood. Here, we review N metabolism first in a “generic” eukaryotic cell, and the contrasting metabolic pathways and regulation of NH4+ and NO3− when these substrates are provided individually under equivalent growth conditions. Then the metabolic interactions of these substrates are described when both are provided together, emphasizing the cellular challenge of balancing nutrient acquisition with photosynthetic energy balance in dynamic environments. Conditions under which dissipatory pathways such as dissimilatory NO3−/ NO2− reduction to NH4+ and photorespiration that may lead to growth suppression are highlighted. While more is known about diatoms, taxon-specific differences in NH4+ and NO3− metabolism that may contribute to changes in phytoplankton community composition when the composition of the N pool changes are presented. These relationships have important implications for harmful algal blooms, development of nutrient criteria for management, and modeling of nutrient uptake by phytoplankton, particularly in conditions where eutrophication is increasing and the redox state of N loads is changing.
453 citations
TL;DR: The properties of the most frequently detected cyanotoxins (namely, microcystins, nodularins, cylindrospermopsin and neurotoxins) are reviewed, describing for each toxin the available information on producing organisms, biosynthesis/genetic and occurrence with a focus on the toxicological profile.
Abstract: Cyanobacteria were present on the earth 3.5 billion years ago; since then they have colonized almost all terrestrial and aquatic ecosystems. They produce a high number of bioactive molecules, among which some are cyanotoxins. Cyanobacterial growth at high densities, forming blooms, is increasing in extension and frequency, following anthropogenic activities and climate changes, giving rise to some concern for human health and animal life exposed to cyanotoxins. Numerous cases of lethal poisonings have been associated with cyanotoxins ingestion in wild animal and livestock. In humans few episodes of lethal or severe human poisonings have been recorded after acute or short-term exposure, but the repeated/chronic exposure to low cyanotoxin levels remains a critical issue. The properties of the most frequently detected cyanotoxins (namely, microcystins, nodularins, cylindrospermopsin and neurotoxins) are here critically reviewed, describing for each toxin the available information on producing organisms, biosynthesis/genetic and occurrence, with a focus on the toxicological profile (including kinetics, acute systemic toxicity, mechanism and mode of action, local effects, repeated toxicity, genotoxicity, carcinogenicity, reproductive toxicity; human health effects and epidemiological studies; animal poisoning) with the derivation of health-based values and considerations on the risks for human health.
379 citations
Cites background from "Environmental conditions that influ..."
...About bloom toxicity, an effect of the environmental conditions on toxin production is undoubtedly plausible, as well as the regulation of mcy genes; however, the exact mechanisms at a molecular level involved in MC production are still not completely clear (Neilan et al. 2012)....
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TL;DR: Analysis of published data suggests that the temperature dependence of the growth rate of cyanob bacteria exceeds that of green algae, and new insights show that the nitrogen-fixation activity of heterocystous cyanobacteria can be strongly stimulated at elevated temperatures.
370 citations
Cites background from "Environmental conditions that influ..."
...These cyanotoxins are less widespread than microcystin, and only a few studies have investigated how their production is affected by environmental conditions (reviewed by Neilan et al., 2013; Boopathi and Ki, 2014)....
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References
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TL;DR: Water used for hemodialysis can contain toxic materials, and its quality should therefore be carefully monitored.
Abstract: Background Hemodialysis is a common but potentially hazardous procedure. From February 17 to 20, 1996, 116 of 130 patients (89 percent) at a dialysis center (dialysis center A) in Caruaru, Brazil, had visual disturbances, nausea, and vomiting associated with hemodialysis. By March 24, 26 of the patients had died of acute liver failure. Methods A case patient was defined as any patient undergoing dialysis at dialysis center A or Caruaru's other dialysis center (dialysis center B) during February 1996 who had acute liver failure. To determine the risk factors for and the source of the outbreak, we conducted a cohort study of the 130 patients at dialysis center A and the 47 patients at dialysis center B, reviewed the centers' water supplies, and collected water, patients' serum, and postmortem liver tissue for microcystin assays. Results One hundred one patients (all at dialysis center A) met the case definition, and 50 died. Affected patients who died were older than those who survived (median age, 47 vs. 3...
1,069 citations
"Environmental conditions that influ..." refers background in this paper
...Several human fatalities have also been reported following acute microcystin poisoning (Jochimsen et al., 1998), while chronic, sublethal doses of microcystin may be carcinogenic (Nishiwaki-Matsushima et al....
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...A study by Saker and Neilan (2001) found that the highest concentrations of cylindrospermopsin in Cylindrospermopsis raciborskii cells occurred when cultures were grown in the absence of a fixed-nitrogen source while the lowest were found in cultures supplied with NH4 as the nitrogen source....
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TL;DR: On May 2, 1878, George Francis of Adelaide, Australia, published the first scholarly description of the potentially lethal e-ects produced by cyanobacteria, sometimes called blue-green algae or, more colloquially, pond scum.
Abstract: On May 2, 1878, George Francis of Adelaide, Australia, published the Þrst scholarly description of the potentially lethal eÝects produced by cyanobacteriaNthe microorganisms sometimes called blue-green algae or, more colloquially, pond scum. In a letter to Nature he noted that an alga he thought to be Nodularia spumigena had so proliferated in the estuary of the Murray River that it had formed a Othick scum like green oil paint, some two to six inches thick, and as thick and pasty as porridge.O This growth had rendered the water OunwholesomeO for cattle and other animals that drink at the surface, bringing on a rapid and sometimes terrible death:
1,002 citations
"Environmental conditions that influ..." refers background in this paper
...This group of alkaloids disrupts acetylcholinesterase activity, causing muscle cell overexcitation and symptoms of cramping, convulsion and respiratory paralysis (Carmichael, 1994)....
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TL;DR: This report is the first complete description of the biosynthesis pathway of a complex cyanobacterial metabolite and represents an integrated polyketide-peptide biosynthetic pathway with a number of unusual structural and enzyme features.
894 citations
"Environmental conditions that influ..." refers background in this paper
...The gene cluster encoding these biosynthetic enzymes has been sequenced and partially characterized in several cyanobacterial genera (Dittmann et al., 1997; Tillett et al., 2000; Christiansen et al., 2003; Rouhiainen et al., 2004)....
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...Elucidation of mcy genes also provided the basis for the construction of various microcystin-deficient mutants (Dittmann et al., 1997; Tillett et al., 2000; Pearson et al., 2004)....
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...It had previously been shown that the mcy gene cluster encodes an ABC transporter, mcyH, putatively involved in toxin export (Tillett et al., 2000; Pearson et al., 2004) (Fig....
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TL;DR: The most effective of these is the antibiotic rifampin (a drug approved for clinical use), which protects mice and rats against microcystin-induced lethality when given prophylactically and, in some cases, therapeutically.
823 citations
Additional excerpts
...(Runnegar et al., 1995; Dawson, 1998)....
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TL;DR: In this paper, the authors showed that microcystin-LR, applied below the acute toxicity level, dose-dependently increases the number and percentage area of positive foci for the placental form of glutathioneS-transferase in rat liver, which was initiated with diethylnitrosamine.
Abstract: Certain waterblooms of toxic cyanobacteria (blue-green algae) are a health threat because of their production of toxic peptides, termed microcystins, which cause liver damage in wild and domesticated animals. The most widely studied microcystin is microcystin-LR, a heptapeptide containing the twol-amino acids, leucine and arginine. The inhibition of protein phosphatase type 1 and type 2A activities by microcystin-LR is similar to that of the known protein phosphatase inhibitor and tumor promoter okadaic acid. We show in this report that microcystin-LR, applied below the acute toxicity level, dose-dependently increases the number and percentage area of positive foci for the placental form of glutathioneS-transferase in rat liver, which was initiated with diethylnitrosamine. The result was obtained independently through two animal experiments. This observation indicates that microcystin-LR is a new liver tumor promoter mediated through inhibition of protein phosphatase type 1 and type 2A activities. This provides further evidence that the okadaic acid pathway is a general mechanism of tumor promotion in various organs, such as mouse skin, rat glandular stomach and rat liver.
743 citations