Effects of secondary metabolites produced by different cyanobacterial populations on the freshwater zooplankters Brachionus calyciflorus and Daphnia pulex

Barbara Pawlik-Skowrońska,Hanna Mazur-Marzec,Magdalena Toporowska

doi:10.1007/s11356-019-04543-1

Abstract

Cyanobacterial blooms in eutrophic water bodies are a worldwide problem. Combined effects of mixtures of secondary metabolites produced by different cyanobacterial species on aquatic fauna are still not well recognised. We compared the survivorship of Brachionus calyciflorus Pallas (Rotifera) and Daphnia pulex Leyding (Cladocera) exposed to pure microcystin LR (MC-LR), anatoxin-a (ANTX) and to five extracts obtained from bloom-forming cyanobacteria Microcystis, Planktothrix and Dolichospermum. The obtained results revealed different response of the organisms to high concentrations of pure MC-LR, ANTX and complex cyanobacterial extracts. The extracts’ toxicity to invertebrates was higher than that exerted by pure cyanotoxins and was dependent on the composition of cyanobacterial metabolites: Microcystis spp. extract containing anabaenopeptins A and B, aeruginosamide, four variants of cyanopeptolins and five MCs was not toxic to either of the organisms, whereas Planktothrix agardhii extract (I), containing anabaenopeptins A, B, F, 915, oscillamide Y, five different aeruginosins and four variants of MC was more toxic to daphnids than to rotifers. The extracts of another P. agarhdii (II) biomass and two different biomass samples of Dolichospermum spp. also affected survivorship of the rotifer and cladoceran, however, to various extent. It strongly suggests that non-ribosomal oligopeptides, other than MCs, had essential contribution to the observed toxicity to invertebrates and their effects on particular species or populations can vary depending on the secondary metabolite profiles of cyanobacteria.

Highlights

Water blooms caused by cyanobacteria are an increasing global problem
We agree with the statement of Ger et al (2014), that since cyanobacteria produce more than one bioactive metabolite, the unsystematic designation of toxicity based on a single well-identified compound is insufficient to assess the environmental impact of cyanobacterial bloom and should be revised
The aim of this work was to compare the effect of pure cyanotoxins (MC-LR, ANTX) and complex mixtures of metabolites produced by different populations of bloom-forming cyanobacterial genera on the survivorship of two freshwater zooplankters of worldwide distribution

Summary

Introduction

Water blooms caused by cyanobacteria are an increasing global problem. Many of the bloom-forming species produce various toxins such as microcystins (MCs), anatoxin-a (ANTX), Responsible editor: Vitor Manuel Oliveira VasconcelosStudies on cyanobacteria-zooplankton interactions have shown diverse and sometimes contradictory results (Tillmanns et al 2008; Ger et al 2014 and references therein). An increasing attention has been paid to the influence of the dissolved fraction of cyanobacterial metabolites on aquatic organisms, including zooplankton (Smutná et al 2014; Ferrão-Filho et al 2014; Barrios et al 2015). During cyanobacterial mass development or cell lysis, especially during bloom collapse, a mixture of toxins and other cyanobacteria cell components occurs in water and can achieve high concentrations. The influence of cyanobacterial metabolites (other than known toxins) on zooplankton reaches an increasing interest (Blom et al 2006; Czarnecki et al 2006; Schwarzenberger et al 2013a; Kohler et al 2014) due to their inhibitory activity to some enzymes such as serine proteases, protein phosphatases, carboxypeptidases. The effects of complex mixtures of cyanobacterial secondary metabolites on zooplankton (and other aquatic organisms) should be thoroughly studied, what was recently strongly emphasised by Barrios et al (2015)

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