Dinophysis toxins: causative organisms, distribution and fate in shellfish

Abstract

Several Dinophysis species produce diarrhoetic toxins (okadaic acid and dinophysistoxins) and pectenotoxins, and cause gastointestinal illness, Diarrhetic Shellfish Poisoning (DSP), even at low cell densities (<103 cells·L⁻¹). They are the main threat, in terms of days of harvesting bans, to aquaculture in Northern Japan, Chile, and Europe. Toxicity and toxin profiles are very variable, more between strains than species. The distribution of DSP events mirrors that of shellfish production areas that have implemented toxin regulations, otherwise misinterpreted as bacterial or viral contamination. Field observations and laboratory experiments have shown that most of the toxins produced by Dinophysis are released into the medium, raising questions about the ecological role of extracelular toxins and their potential uptake by shellfish. Shellfish contamination results from a complex balance between food selection, adsorption, species-specific enzymatic transformations, and allometric processes. Highest risk areas are those combining Dinophysis strains with high cell content of okadaates, aquaculture with predominance of mytilids (good accumulators of toxins), and consumers who frequently include mussels in their diet. Regions including pectenotoxins in their regulated phycotoxins will suffer from much longer harvesting bans and from disloyal competition with production areas where these toxins have been deregulated.

Figure 1

Chemical structure of (A) okadaic acid and its congeners (OAs) and (B) pectenotoxins (PTXs). A dashed line in the link O–C33 indicates where hydrolysis to produce pectenotoxin seco-acids (PTX-SA) takes place.

Figure 2

Micrographs of toxin-containing (reported so far) Dinophysis and Phalacroma species. (A) D. acuta; (B) D. acuminata; (C) D. sacculus; (D) D. Fortii; (E) D. norvegica; (F) Phalacroma mitra; (G) D. ovum; (H) P. rotundatum; (I) D. infundibula; (J) D. tripos; (K) D. caudata; and (L) D. miles. All live/fixed specimens from the Galician Rías (Northwest Spain) except H, which is from the Gullmar Fjord (Sweden), and F and L, tropical specimens courtesy of J. Larsen. Scale bar = 20 µm (Note: C is reprinted with permission from [47], copyright © 2013 Elsevier).

Figure 3

Global distribution of geo-referenced locations where Dinophysis toxins have been detected, including cases where they were below regulatory levels. Created with references cited in the text and additional information from the ICES-IOC Harmful Algae events Database (HAEDAT) [180].

Figure 4

Duration of mussel (M. galloprovincialis) harvesting bans in different production areas within the Galician Rías, Northwest Spain. Data are from 2000, coinciding with persistent high densities of D. acuminata from February to November [182].

Figure 5

Distribution of geo-referenced locations where Dinophysis toxins have been detected, including cases where they were below regulatory level, in Europe.

Figure 6

Distribution of geo-referenced locations where Dinophysis toxins have been detected, including cases where they were below RL, in the West Pacific region.

Figure 7

Distribution of geo-referenced locations where Dinophysis toxins have been detected, including cases where they were below RL, in South America.

Figure 8

(A) Theoretical toxin accumulation by bivalves and (B) proportion of ingested toxin that is accumulated, assuming a clearance rate of 3 L·h⁻¹, an absorption efficiency of 100%, and two toxin concentrations in seston: 1000 pg·L⁻¹ (red line) and 4000 pg·L⁻¹ (black line). These represent, for example, the combination of a Dinophysis density of 100 cells·L⁻¹ and a cell toxin quota of 10 pg, in the first case, and of 100 cells·L⁻¹ and a cell toxin quota of 40 pg or 400 cells·L⁻¹ with 10 pg of toxin·cell⁻¹, in the second case. The body weight of the bivalve was assumed to be 10 g, and two depuration rates were used: 0.05 (continuous lines) and 0.10 (dashed lines) day⁻¹.

Figure 9

Main transformations of the toxins of the okadaic acid group. Labels inside the boxes indicate the moieties that constitute the molecule. Zigzag lines indicate the bonds that are broken to generate other compounds. The line(s) of each box indicate whether the compounds are found in phytoplankton or in bivalves.

Figure 10

(A) Theoretical evolution of different esters of okadaic acid after a toxic bloom [12]; (B,C) some examples in which the maximum of free toxins appears after the maximum of esters during a natural bloom [273]; and (D) increase in free toxin (especially when no food was supplied) during an depuration experiment in the laboratory [291] (Note: B and C reprinted with permission from [273], copyright © Elsevier, 2005; and D reprinted with permission from [291], copyright © Elsevier, 2003).