The Individual and Combined Effects of the Cyanotoxins, Anatoxin-a and Microcystin-LR, on the Growth, Toxin Production, and Nitrogen Fixation of Prokaryotic and Eukaryotic Algae.

Mathias Chia,Maria Bittencourt-Oliveira,Christopher Gobler,Jennifer Jankowiak,Benjamin Kramer

doi:10.3390/toxins11010043

Mathias Chia, Maria Bittencourt-Oliveira + Show 3 more

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https://doi.org/10.3390/toxins11010043

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Abstract

Globally, eutrophication and warming of aquatic ecosystems has increased the frequency and intensity of cyanobacterial blooms and their associated toxins, with the simultaneous detection of multiple cyanotoxins often occurring. Despite the co-occurrence of cyanotoxins such as microcystins and anatoxin-a (ATX) in water bodies, their effects on phytoplankton communities are poorly understood. The individual and combined effects of microcystin-LR (MC-LR) and ATX on the cyanobacteria Microcystis spp., and Anabaena variabilis (a.k.a. Trichormus variabilis), and the chlorophyte, Selenastrum capricornutum were investigated in the present study. Cell density, chlorophyll-a content, and the maximum quantum efficiency of photosystem II (Fv/Fm) of Microcystis cells were generally lowered after exposure to ATX or MC-LR, while the combined treatment with MC-LR and ATX synergistically reduced the chlorophyll-a concentration of Microcystis strain LE-3. Intracellular levels of microcystin in Microcystis LE-3 significantly increased following exposure to MC-LR + ATX. The maximum quantum efficiency of photosystem II of Anabaena strain UTEX B377 declined during exposure to the cyanotoxins. Nitrogen fixation by Anabaena UTEX B377 was significantly inhibited by exposure to ATX, but was unaffected by MC-LR. In contrast, the combination of both cyanotoxins (MC-LR + ATX) caused a synergistic increase in the growth of S. capricornutum. While the toxins caused an increase in the activity of enzymes that scavenge reactive oxygen species in cyanobacteria, enzyme activity was unchanged or decreased in S. capricornutum. Collectively this study demonstrates that MC-LR and ATX can selectively promote and inhibit the growth and performance of green algae and cyanobacteria, respectively, and that the combined effect of these cyanotoxins was often more intense than their individual effects on some strains. This suggests that the release of multiple cyanotoxins in aquatic ecosystems, following the collapse of blooms, may influence the succession of plankton communities.

Highlights

Aquatic ecosystems are characterized by different communities of plants and animals that interact with each other and the abiotic environment
Microcystin-LR (MC-LR) and ATX were stimulatory to Selenastrum capricornutum and may facilitate its dominance following the collapse of toxic cyanobacteria blooms
These results demonstrate that the presence of more than one cyanotoxin in the environment can have synergistic

Summary

Introduction

Aquatic ecosystems are characterized by different communities of plants and animals that interact with each other and the abiotic environment. Increasing nutrient concentrations can alter plankton communities and promote the formation of algal and cyanobacterial blooms [3,4,5]. Cyanobacterial blooms are a worldwide environmental problem due the production of cyanotoxins, which include hepatotoxins, neurotoxins, cytotoxins, and dermatoxins which inhibit protein synthesis and phosphatase activities, irreversibly block acetylcholinesterase, promote tumor formation, and cause skin problems, respectively [6,7,8]. Higher concentrations of cyanotoxins are being detected in aquatic ecosystems, a scenario that may have broad effects on the ecology of plants and animals in different environments [9]

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