The Cost of Toxicity in Microalgae: Direct Evidence From the Dinoflagellate Alexandrium.

Hannah E. Blossom,Niels Daugbjerg,Bo Markussen,Andreas Norlin,Bernd Krock,Per Juel Hansen

doi:10.3389/fmicb.2019.01065

Abstract

Empirical evidence of the cost of producing toxic compounds in harmful microalgae is completely lacking. Yet costs are often assumed to be high, implying substantial ecological benefits with adaptive significance exist. To study potential fitness costs of toxin production, 16 strains including three species of the former Alexandrium tamarense species complex were grown under both carbon limitation and unlimited conditions. Growth rates, levels of intracellular paralytic shellfish toxins (PSTs), and effects of lytic compounds were measured to provide trade-off curves of toxicity for both PST and lytic toxicity under high light (300 μmol photons m−2 s−1) and under low light (i.e., carbon limited; 20 μmol photons m−2 s−1). Fitness costs in terms of reduced growth rates with increasing PST content were only evident under unlimited conditions, but not under carbon limitation, in which case PST production was positively correlated with growth. The cost of production of lytic compounds was detected both under carbon limitation and unlimited conditions, but only in strains producing PST. The results may direct future research in understanding the evolutionary role and ecological function of algal toxins. The intrinsic growth rate costs should be accounted for in relation to quantifying benefits such as grazer avoidance or toxin-mediated prey capture in natural food web settings.

Highlights

The microalgae responsible for harmful algal blooms (HABs) produce a wide variety of bioactive natural products, or secondary metabolites, known as phycotoxins (Smayda, 1997; Cembella, 2003)
Many HAB species produce toxins, referred to as lytic compounds or allelochemicals, which can be released into the surrounding environment, where they cause cell lysis and death of other planktonic organisms
The trade-off of lytic toxicity with growth was more pronounced at LL than at high light (HL) (LL compared to HL; Figures 5A,B), indicating costs are inflated at low light when strains were subject to carbon limitation

Summary

Introduction

The microalgae responsible for harmful algal blooms (HABs) produce a wide variety of bioactive natural products, or secondary metabolites, known as phycotoxins (Smayda, 1997; Cembella, 2003). In contrast to the known phycotoxins previously mentioned, the lytic compounds have a more direct ecological role as toxins because they cause cell lysis of algal competitors and protist grazers This chemically induced interference competition is a concept known as allelopathy, well described in terrestrial plants (Molish, 1937). In an aqueous medium governed by dilution, turbulence, and viscous forces, a released compound may never reach the intended target in relevant concentrations, and a threshold density of lytic algae must be reached to elicit an effect (Jonsson et al, 2009) Because of this and the potential for non-toxic individuals to receive a benefit, without suffering the cost of producing lytic compounds, the selective driving forces for allelopathy as an adaptive competitive strategy have been challenged (Lewis, 1986; Jonsson et al, 2009). The evolutionary role and ecological function of lytic compounds have become unclear

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Conclusion