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

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.

Neurotoxic Anatoxin-a Can Also Exert Immunotoxicity by the Induction of Apoptosis on Carassius auratus Lymphocytes in vitro When Exposed to Environmentally Relevant Concentrations

“…Animals reportedly die from exposure to ANTX-a following toxic response to acetylcholine receptor inhibition at neuromuscular junction (Carneiro et al, 2015). Chia et al (2019) revealed that high-dose injection or ingestion of ANTXa can cause fatal suffocation in mammals and induces oxidative stress. The influence of ANTX-a on the biological nervous system has been extensively investigated because ANTX-a is toxic to this system; nervous system diseases are characterized by disordered muscle bundles, decreased motor ability, tremor and gait changes, irregular breathing (Rymuszka and Sieroslawska, 2009).…”

Effects of Microcystin-LR on the Microstructure and Inflammation-Related Factors of Jejunum in Mice

“…The rapid development of industries and agriculture has led to the increasing discharge of wastewater containing nitrogen and phosphorus into water bodies. These activities may result in eutrophication and development of cyanobacterial blooms [1,2]. The monocyclic heptapeptide microcystins (MCs) are the secondary products of cyanobacteria metabolism and most harmful cyanotoxin found in water bodies [3,4,5].…”

Reviewing Interspecies Interactions as a Driving Force Affecting the Community Structure in Lakes via Cyanotoxins

“…Chia et al [ 145 ] studied the effects of the cyanotoxins ATX-a and MC-LR as single toxins and combinations of both (25 µg L −1 each) on Microcystis spp., T. variabilis and the green alga Selenastrum capricornutum . Following exposure to the cyanotoxins, ATX-a or MC-LR, the growth of Microcystis LE-3 was inhibited.…”

“…These data demonstrated the diverse effects of cyanotoxins on the growth and physiology of phytoplankton species, which may explain the succession of the green algae following the collapse of toxic cyanobacterial blooms. Even though species-specific effects related to the cyanotoxins individually and combined were observed, the effects of the combined toxins on some strains were greater than with single toxin exposures [ 145 ].…”