Daphnia's Adaptive Molecular Responses to the Cyanobacterial Neurotoxin Anatoxin-α Are Maternally Transferred.

Anke Schwarzenberger,Dominik Martin-Creuzburg

doi:10.3390/toxins13050326

Abstract

Cyanobacterial blooms are an omnipresent and well-known result of eutrophication and climate change in aquatic systems. Cyanobacteria produce a plethora of toxic secondary metabolites that affect humans, animals and ecosystems. Many cyanotoxins primarily affect the grazers of phytoplankton, e.g., Daphnia. The neurotoxin anatoxin-α has been reported world-wide; despite its potency, anatoxin-α and its effects on Daphnia have not been thoroughly investigated. Here, we investigated the effects of the anatoxin-α-producing Tychonema on life-history parameters and gene expression of nicotine-acetylcholine receptors (NAR), the direct targets of anatoxin-α, using several D. magna clones. We used juvenile somatic growth rates as a measure of fitness and analyzed gene expression by qPCR. Exposure to 100% Tychonema reduced the clones’ growth rates and caused an up-regulation of NAR gene expression. When 50% of the food consisted of Tychonema, none of the clones were reduced in growth and only one of them showed an increase in NAR gene expression. We demonstrate that this increased NAR gene expression can be maternally transferred and that offspring from experienced mothers show a higher growth rate when treated with 50% Tychonema compared with control offspring. However, the addition of further (anthropogenic) stressors might impair Daphnia’s adaptive responses to anatoxin-α. Especially the presence of certain pollutants (i.e., neonicotinoids), which also target NARs, might reduce Daphnia’s capability to cope with anatoxin-α.

Highlights

Over the last decades, cyanobacterial blooms have increased in frequency in freshwater ecosystems because of the combined effects of eutrophication, global warming, and low riverflows due to drought conditions [1]
When 50% of the food consisted of Tychonema, none of the clones were reduced in growth and only one of them showed an increase in nicotine-acetylcholine receptors (NAR) gene expression
We demonstrate that this increased NAR gene expression can be maternally transferred and that offspring from experienced mothers show a higher growth rate when treated with 50% Tychonema compared with control offspring

Summary

Introduction

Cyanobacterial blooms have increased in frequency in freshwater ecosystems because of the combined effects of eutrophication, global warming, and low riverflows due to drought conditions [1]. One exceptionally dangerous toxin for humans, livestock and wildlife is the Very Fast Death Factor [4,5]—the neurotoxic alkaloid anatoxin-α. This toxin acts very quickly on the nervous system and an antidote is unknown. Anatoxin-α has been observed in natural lake blooms globally [6,7,8,9,10,11,12] It is produced by different cyanobacterial species, e.g., Tychonema [12], Anabaena [7,13,14], Pseudoanabaena, Planktothrix [7] and Aphanizomenon [15]. The management of cyanobacterial blooms with anatoxin-α is crucial because this toxin is a concern for human, animal and ecosystem health [6], and because anatoxin-α has already been found in dietary supplements containing cyanobacteria [16]

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