Distribution and abundance of azaspiracid-producing dinophyte species and their toxins in North Atlantic and North Sea waters in summer 2018.

Stephan Wietkamp,Daniela Voß,Jane Kilcoyne,Rafael Salas,Dave Clarke,Urban Tillmann,Bernd Krock

doi:10.1371/journal.pone.0235015

Abstract

Representatives of the marine dinophyte family Amphidomataceae produce lipophilic phycotoxins called azaspiracids (AZA) which may cause azaspiracid shellfish poisoning (AZP) in humans after consumption of contaminated seafood. Three of the four known toxigenic species are observed frequently in the eastern North Atlantic. In 2018, a research survey was performed to strengthen knowledge on the distribution and abundance of toxigenic Amphidomataceae and their respective toxins in Irish coastal waters and in the North Sea. Species-specific quantification of the three toxigenic species (Azadinium spinosum, Azadinium poporum and Amphidoma languida) was based on recently developed qPCR assays, whose performance was successfully validated and tested with specificity tests and spike experiments. The multi-method approach of on-board live microscopy, qPCR assays and chemical AZA-analysis revealed the presence of Amphidomataceae in the North Atlantic including the three targeted toxigenic species and their respective AZA analogues (AZA-1, -2, -33, -38, -39). Azadinium spinosum was detected at the majority of Irish stations with a peak density of 8.3 x 104 cells L-1 and AZA (AZA-1, -2, -33) abundances up to 1,274 pg L-1. Amphidoma languida was also present at most Irish stations but appeared in highest abundance in a bloom at a central North Sea station with a density of 1.2 x 105 cells L-1 and an AZA (AZA-38, -39) abundances of 618 pg L-1. Azadinium poporum was detected sporadically at the Irish south coast and North Sea and was rather low in abundance during this study. The results confirmed the wide distribution and frequent occurrence of the target species in the North Atlantic area and revealed, for the first time, bloom abundances of toxigenic Amphidomataceae in this area. This emphasizes the importance of future studies and monitoring of amphidomatacean species and their respective AZA analogues in the North Atlantic.

Highlights

Marine toxic microalgae are of concern for human health and aquaculture industries worldwide
Mean temperature (S1A Fig ) of the upper layer was highest in the German Bight and the North Sea entrance of the English Channel, reaching 18.5 ̊C at Helgoland and 18.9 ̊C at station 4
Microscopy, species-specific quantitative polymerase chain reaction (qPCR) assays and LC-MS/MS revealed that Amphidomataceae, and especially all three North Atlantic toxigenic species, are widely distributed in Irish coastal waters, the Celtic Sea and the North Sea

Summary

Introduction

Marine toxic microalgae are of concern for human health and aquaculture industries worldwide. Higher cell densities of harmful algae may occur at any time of the year, when conditions are favorable, but the complex interplay of both biotic and abiotic factors determining these outbreaks are still not fully understood [1, 2] These harmful algal blooms can cause the death of aquatic organisms, including large fish-kills, or may lead to accumulation of toxic compounds within the aquatic food web. Well-known examples of those toxic algal compounds are yessotoxins (YTX, produced by e.g., Protoceratium reticulatum), diarrhetic-shellfish-poisoning toxins (DSP, produced by e.g., Dinophysis spp.) and paralytic-shellfish-poisoning toxins (PSP, produced by e.g., Alexandrium spp.) [4–7] While these toxins have been thoroughly studied since the 1970s and 80s, another group of microalgal toxins, azaspiracids (AZA), which were more recently discovered [8], are known to accumulate in shellfish. AZA were found, for the first time, along the Atlantic coast of southern Spain with elevated levels observed in molluscan shellfish [13]

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