Toward Disentangling the Multiple Nutritional Constraints Imposed by Planktothrix: The Significance of Harmful Secondary Metabolites and Sterol Limitation.

Anke Schwarzenberger,Dominik Martin-Creuzburg,Rainer Kurmayer

doi:10.3389/fmicb.2020.586120

Anke Schwarzenberger, Dominik Martin-Creuzburg + Show 1 more

Open Access

https://doi.org/10.3389/fmicb.2020.586120

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Abstract

The harmful bloom-forming cyanobacterium Planktothrix is commonly considered to be nutritionally inadequate for zooplankton grazers, resulting in limited top-down control. However, interactions between Planktothrix and zooplankton grazers are poorly understood. The food quality of Planktothrix is potentially constrained by morphological properties (i.e., filament formation), the production of harmful secondary metabolites, and a deficiency in essential lipids (i.e., primarily sterols). Here, we investigated the relative significance of toxin production (microcystins, carboxypeptidase A inhibitors, protease inhibitors) and sterol limitation for the performance of Daphnia feeding on one Planktothrix rubescens and one P. agardhii wild-type/microcystin knock-out mutant pair. Our data suggest that the poor food quality of both Planktothrix spp. is due to deleterious effects mediated by various harmful secondary metabolites and that the impact of sterol limitation is partially or completely superimposed by toxicity. The significance of the different factors seems to depend on the metabolite profile of the considered Planktothrix strain and the Daphnia clone that is used for the experiments. The toxin-responsive gene expression (transporter genes, gpx, and trypsin) and enzyme activity patterns revealed strain-specific food quality constraints and that Daphnia is capable of modulating its physiological responses according to the ingested Planktothrix strain. Future studies need to consider that Planktothrix–grazer interactions are simultaneously modulated by multiple factors to improve our understanding of top-down influences on Planktothrix bloom formation.

Highlights

Cyanobacteria of the genus Planktothrix are widely distributed in lakes (Kurmayer et al, 2011) and well-known to produce secondary metabolites that are potentially harmful for human health and livestock (Rohrlack et al, 2005; Kohler et al, 2014; Kurmayer et al, 2015)
Our experiments indicate that the impact of sterol limitation on Daphnia performance is partially or completely superimposed by toxicity, depending on the Planktothrix strain and the Daphnia clone studied
Despite pronounced differences in metabolite composition, the two Planktothrix WT strains hardly differed in food quality, i.e., they all resulted in similar low somatic growth rates of D. magna

Summary

Introduction

Cyanobacteria of the genus Planktothrix are widely distributed in lakes (Kurmayer et al, 2011) and well-known to produce secondary metabolites that are potentially harmful for human health and livestock (Rohrlack et al, 2005; Kohler et al, 2014; Kurmayer et al, 2015). Planktothrix has become the predominant photoautotrophic organism in many temperate. The success of Planktothrix in past decades has been attributed to a combination of physico-chemical and ecological changes, i.e., longer stratification period due to lake warming, increased water transparency due to decreasing phosphorus loads and decreasing phytoplankton biomass, and an advantage over other phytoplankton species that are less competitive for phosphorus (Jacquet et al, 2005, 2014; Posch et al, 2012)

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