A molecular and co-evolutionary context for grazer induced toxin production in Alexandrium tamarense.

Sylke Wohlrab,Morten H Iversen,Uwe John,Lars-Anders Hansson

doi:10.1371/journal.pone.0015039

Abstract

Marine dinoflagellates of the genus Alexandrium are the proximal source of neurotoxins associated with Paralytic Shellfish Poisoning. The production of these toxins, the toxin biosynthesis and, thus, the cellular toxicity can be influenced by abiotic and biotic factors. There is, however, a lack of substantial evidence concerning the toxins' ecological function such as grazing defense. Waterborne cues from copepods have been previously found to induce a species-specific increase in toxin content in Alexandrium minutum. However, it remains speculative in which context these species-specific responses evolved and if it occurs in other Alexandrium species as well. In this study we exposed Alexandrium tamarense to three copepod species (Calanus helgolandicus, Acartia clausii, and Oithona similis) and their corresponding cues. We show that the species-specific response towards copepod-cues is not restricted to one Alexandrium species and that co-evolutionary processes might be involved in these responses, thus giving additional evidence for the defensive role of phycotoxins. Through a functional genomic approach we gained insights into the underlying molecular processes which could trigger the different outcomes of these species-specific responses and consequently lead to increased toxin content in Alexandrium tamarense. We propose that the regulation of serine/threonine kinase signaling pathways has a major influence in directing the external stimuli i.e. copepod-cues, into different intracellular cascades and networks in A. tamarense. Our results show that A. tamarense can sense potential predating copepods and respond to the received information by increasing its toxin production. Furthermore, we demonstrate how a functional genomic approach can be used to investigate species interactions within the plankton community.

Highlights

Dinoflagellates of the genus Alexandrium possess a high ecological impact due to their ability to form Harmful Algal Blooms associated with Paralytic Shellfish Poisoning (PSP)
Additional evidence of Paralytic Shellfish Toxins (PST) acting as grazer defense compounds is given by Selander et al [28], who demonstrated that PST content was increased in Alexandrium minutum after exposure to waterborne cues from copepods, which correlated with a decreased copepod grazing
Bergkvist et al [29] found that A. minutum only increased its PST production significantly when exposed to waterborne cues from two out of three different copepods, which indicates that toxin production might be target specific

Summary

Introduction

Dinoflagellates of the genus Alexandrium possess a high ecological impact due to their ability to form Harmful Algal Blooms associated with Paralytic Shellfish Poisoning (PSP). Studies focusing on the influence of copepod grazing on dinoflagellates have shown both (1) high ingestion rates of toxic Alexandrium with no adverse effects on the grazers as well as (2) enhanced mortality of the grazer [16,17]. It seems that grazing experiments are highly dependent on the Alexandrium strain investigated, as well as on the grazer species [11]. Naturally occurring Alexandrium populations are composed of different strains, producing different amounts of PST, and possessing different PST profiles [22] Such genotypic and phenotypic diversity could lead to varying results among grazing studies. Bergkvist et al [29] found that A. minutum only increased its PST production significantly when exposed to waterborne cues from two out of three different copepods, which indicates that toxin production might be target specific

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