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4 pages, 207 KiB

Open AccessEditorial

Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts

by Beatriz Reguera and Juan Blanco

Toxins 2019, 11(7), 413; https://doi.org/10.3390/toxins11070413 - 16 Jul 2019

Cited by 9 | Viewed by 3304

Abstract

Several planktonic dinoflagellate species of the genus Dinophysis produce one or two groups of lipophilic toxins: (i) okadaic acid (OA) and its derivatives, the dinophysistoxins (DTXs), and (ii) pectenotoxins (PTXs) [...] Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

Research

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28 pages, 6126 KiB

Open AccessEditor’s ChoiceArticle

Dinophysis Species and Diarrhetic Shellfish Toxins: 20 Years of Monitoring Program in Andalusia, South of Spain

by Raúl Fernández, Luz Mamán, David Jaén, Lourdes Fernández Fuentes, M. Asunción Ocaña and M. Mercedes Gordillo

Toxins 2019, 11(4), 189; https://doi.org/10.3390/toxins11040189 - 29 Mar 2019

Cited by 22 | Viewed by 4182

Abstract

In Andalusia, the official monitoring program for toxic phytoplankton and marine biotoxins was launched in 1994 to comply with European legislation. Since then, there have been numerous episodes of DST (Diarrhetic shellfish toxins) associated with the proliferation of Dinophysis species. This article reviews [...] Read more.

In Andalusia, the official monitoring program for toxic phytoplankton and marine biotoxins was launched in 1994 to comply with European legislation. Since then, there have been numerous episodes of DST (Diarrhetic shellfish toxins) associated with the proliferation of Dinophysis species. This article reviews two decades of time series data and assesses the effectiveness of the program established. The testing of lipophilic toxins and toxic phytoplankton is based on official methods harmonized and accredited since 2007 according to the standard UNE-EN-ISO 17025. The major species of Dinophysis identified were D. acuminata complex, D. caudata, D. acuta and D. fortii, with the main growth season being from early spring until the end of autumn. Both D. acuminata complex and D. acuta have been clearly associated with toxicity in molluscs. Despite the complexity of data obtained through monitoring programs, it is possible to provide early warning of potential health risks for most situations. This is the first report of Dinophysis species and their relation to DST events in a time series from Andalusia. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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18 pages, 5809 KiB

Open AccessArticle

A Long-Term Time Series of Dinophysis acuminata Blooms and Associated Shellfish Toxin Contamination in Port Underwood, Marlborough Sounds, New Zealand

by Lincoln A. Mackenzie

Toxins 2019, 11(2), 74; https://doi.org/10.3390/toxins11020074 - 1 Feb 2019

Cited by 19 | Viewed by 4613

Abstract

Blooms of the dinoflagellate Dinophysis acuminata occur every year in an important mussel cultivation area in Port Underwood, Marlborough Sounds, New Zealand. Annual maximum cell numbers range from 1500–75,000 cells L⁻¹ and over 25 years of weekly monitoring the D. acuminata bloom [...] Read more.

Blooms of the dinoflagellate Dinophysis acuminata occur every year in an important mussel cultivation area in Port Underwood, Marlborough Sounds, New Zealand. Annual maximum cell numbers range from 1500–75,000 cells L⁻¹ and over 25 years of weekly monitoring the D. acuminata bloom has never failed to exhibit peaks in abundance at some time between spring and autumn. During winter (June–August) the dinoflagellate is often undetectable, or at low levels (≤100 cells L⁻¹), and the risk of diarrhetic shellfish poisoning (DSP)-toxin contamination over this period is negligible. Bloom occurrence may be coupled to the abundance of D. acuminata prey (Mesodinium sp.) but the mechanism by which it maintains its long-term residence in this hydrologically dynamic environment is unknown. The toxin profile of D. acuminata is dominated by pectenotoxin-2 (PTX-2) and dinophysistoxin-1 (DTX-1), but the cellular toxin content is low. It is rare that free DTX-1 is detected in mussels as this is invariably exclusively present as fatty acid-esters. In only five out of >2500 mussel samples over 16 years have the levels of total DTX-1 marginally exceeded the regulated level of 0.16 mg kg⁻¹. It is also rare that free PTX-2 is detected in mussels, as it is generally only present in its hydrolysed non-toxic PTX-2 seco acid form. The D. acuminata alert level of 1000 cells L⁻¹ is often exceeded without DTX-1 residues increasing appreciably, and this level is considered too conservative. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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16 pages, 730 KiB

Open AccessArticle

Prey Lysate Enhances Growth and Toxin Production in an Isolate of Dinophysis acuminata

by Han Gao, Mengmeng Tong, Xinlong An and Juliette L. Smith

Toxins 2019, 11(1), 57; https://doi.org/10.3390/toxins11010057 - 21 Jan 2019

Cited by 4 | Viewed by 3906

Abstract

The physiological and toxicological characteristics of Dinophysis acuminata have been increasingly studied in an attempt to better understand and predict diarrhetic shellfish poisoning (DSP) events worldwide. Recent work has identified prey quantity, organic nitrogen, and ammonium as likely contributors to increased Dinophysis growth [...] Read more.

The physiological and toxicological characteristics of Dinophysis acuminata have been increasingly studied in an attempt to better understand and predict diarrhetic shellfish poisoning (DSP) events worldwide. Recent work has identified prey quantity, organic nitrogen, and ammonium as likely contributors to increased Dinophysis growth rates and/or toxicity. Further research is now needed to better understand the interplay between these factors, for example, how inorganic and organic compounds interact with prey and a variety of Dinophysis species and/or strains. In this study, the exudate of ciliate prey and cryptophytes were investigated for an ability to support D. acuminata growth and toxin production in the presence and absence of prey, i.e., during mixotrophic and phototrophic growth respectively. A series of culturing experiments demonstrated that the addition of ciliate lysate led to faster dinoflagellate growth rates (0.25 ± 0.002/d) in predator-prey co-incubations than in treatments containing (1) similar levels of prey but without lysate (0.21 ± 0.003/d), (2) ciliate lysate but no live prey (0.12 ± 0.004/d), or (3) monocultures of D. acuminata without ciliate lysate or live prey (0.01 ± 0.007/d). The addition of ciliate lysate to co-incubations also resulted in maximum toxin quotas and extracellular concentrations of okadaic acid (OA, 0.11 ± 0.01 pg/cell; 1.37 ± 0.10 ng/mL) and dinophysistoxin-1 (DTX1, 0.20 ± 0.02 pg/cell; 1.27 ± 0.10 ng/mL), and significantly greater total DSP toxin concentrations (intracellular + extracellular). Pectenotoxin-2 values, intracellular or extracellular, did not show a clear trend across the treatments. The addition of cryptophyte lysate or whole cells, however, did not support dinoflagellate cell division. Together these data demonstrate that while certain growth was observed when only lysate was added, the benefits to Dinophysis were maximized when ciliate lysate was added with the ciliate inoculum (i.e., during mixotrophic growth). Extrapolating to the field, these culturing studies suggest that the presence of ciliate exudate during co-occurring dinoflagellate-ciliate blooms may indirectly and directly exacerbate D. acuminata abundance and toxigenicity. More research is required, however, to understand what direct or indirect mechanisms control the predator-prey dynamic and what component(s) of ciliate lysate are being utilized by the dinoflagellate or other organisms (e.g., ciliate or bacteria) in the culture if predictive capabilities are to be developed and management strategies created. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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21 pages, 5601 KiB

Open AccessEditor’s ChoiceArticle

Mesoscale Dynamics and Niche Segregation of Two Dinophysis Species in Galician-Portuguese Coastal Waters

by Patricio A. Díaz, Beatriz Reguera, Teresa Moita, Isabel Bravo, Manuel Ruiz-Villarreal and Santiago Fraga

Toxins 2019, 11(1), 37; https://doi.org/10.3390/toxins11010037 - 14 Jan 2019

Cited by 20 | Viewed by 3697

Abstract

Blooms of Dinophysis acuminata occur every year in Galicia (northwest Spain), between spring and autumn. These blooms contaminate shellfish with lipophilic toxins and cause lengthy harvesting bans. They are often followed by short-lived blooms of Dinophysis acuta, associated with northward longshore transport, [...] Read more.

Blooms of Dinophysis acuminata occur every year in Galicia (northwest Spain), between spring and autumn. These blooms contaminate shellfish with lipophilic toxins and cause lengthy harvesting bans. They are often followed by short-lived blooms of Dinophysis acuta, associated with northward longshore transport, at the end of the upwelling season. During the summers of 1989 and 1990, dense blooms of D. acuta developed in situ, initially co-occurring with D. acuminata and later with the paralytic shellfish toxin-producer Gymnodinium catenatum. Unexplored data from three cruises carried out before, during, and following autumn blooms (13–14, 27–28 September and 11–12 October) in 1990 showed D. acuta distribution in shelf waters within the 50 m and 130 m isobaths, delimited by the upwelling front. A joint review of monitoring data from Galicia and Portugal provided a mesoscale view of anomalies in SST and other hydroclimatic factors associated with a northward displacement of the center of gravity of D. acuta populations. At the microscale, re-examination of the vertical segregation of cell maxima in the light of current knowledge, improved our understanding of niche differentiation between the two species of Dinophysis. Results here improve local transport models and forecast of Dinophysis events, the main cause of shellfish harvesting bans in the most important mussel production area in Europe. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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23 pages, 2325 KiB

Open AccessEditor’s ChoiceArticle

Interannual Variability of Dinophysis acuminata and Protoceratium reticulatum in a Chilean Fjord: Insights from the Realized Niche Analysis

by Catharina Alves-de-Souza, José Luis Iriarte and Jorge I. Mardones

Toxins 2019, 11(1), 19; https://doi.org/10.3390/toxins11010019 - 5 Jan 2019

Cited by 29 | Viewed by 4420

Abstract

Here, we present the interannual distribution of Dinophysis acuminata and Protoceratium reticulatum over a 10-year period in the Reloncaví Fjord, a highly stratified fjord in southern Chile. A realized subniche approach based on the Within Outlying Mean Index (WitOMI) was used to decompose [...] Read more.

Here, we present the interannual distribution of Dinophysis acuminata and Protoceratium reticulatum over a 10-year period in the Reloncaví Fjord, a highly stratified fjord in southern Chile. A realized subniche approach based on the Within Outlying Mean Index (WitOMI) was used to decompose the species’ realized niche into realized subniches (found within subsets of environmental conditions). The interannual distribution of both D. acuminata and P. reticulatum summer blooms was strongly influenced by climatological regional events, i.e., El Niño Southern Oscillation (ENSO) and the Southern Annual Mode (SAM). The two species showed distinct niche preferences, with blooms of D. acuminata occurring under La Niña conditions (cold years) and low river streamflow whereas P. reticulatum blooms were observed in years of El Niño conditions and positive SAM phase. The biological constraint exerted on the species was further estimated based on the difference between the existing fundamental subniche and the realized subniche. The observed patterns suggested that D. acuminata was subject to strong biological constraint during the studied period, probably as a result of low cell densities of its putative prey (the mixotrophic ciliate Mesodinium cf. rubrum) usually observed in the studied area. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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22 pages, 4341 KiB

Open AccessArticle

Notes on the Cultivation of Two Mixotrophic Dinophysis Species and Their Ciliate Prey Mesodinium rubrum

by Jorge Hernández-Urcera, Pilar Rial, María García-Portela, Patricia Lourés, Jane Kilcoyne, Francisco Rodríguez, Amelia Fernández-Villamarín and Beatriz Reguera

Toxins 2018, 10(12), 505; https://doi.org/10.3390/toxins10120505 - 1 Dec 2018

Cited by 16 | Viewed by 4014

Abstract

Kleptoplastic mixotrophic species of the genus Dinophysis are cultured by feeding with the ciliate Mesodinium rubrum, itself a kleptoplastic mixotroph, that in turn feeds on cryptophytes of the Teleaulax/Plagioselmis/Geminigera (TPG) clade. Optimal culture media for phototrophic growth of [...] Read more.

Kleptoplastic mixotrophic species of the genus Dinophysis are cultured by feeding with the ciliate Mesodinium rubrum, itself a kleptoplastic mixotroph, that in turn feeds on cryptophytes of the Teleaulax/Plagioselmis/Geminigera (TPG) clade. Optimal culture media for phototrophic growth of D. acuminata and D. acuta from the Galician Rías (northwest Spain) and culture media and cryptophyte prey for M. rubrum from Huelva (southwest Spain) used to feed Dinophysis, were investigated. Phototrophic growth rates and yields were maximal when D. acuminata and D. acuta were grown in ammonia-containing K(-Si) medium versus f/2(-Si) or L1(-Si) media. Dinophysis acuminata cultures were scaled up to 18 L in a photobioreactor. Large differences in cell toxin quota were observed in the same Dinophysis strains under different experimental conditions. Yields and duration of exponential growth were maximal for M. rubrum from Huelva when fed Teleaulax amphioxeia from the same region, versus T. amphioxeia from the Galician Rías or T. minuta and Plagioselmis prolonga. Limitations for mass cultivation of northern Dinophysis strains with southern M. rubrum were overcome using more favorable (1:20) Dinophysis: Mesodinium ratios. These subtleties highlight the ciliate strain-specific response to prey and its importance to mass production of M. rubrum and Dinophysis cultures. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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8 pages, 1335 KiB

Open AccessArticle

First Report of Okadaic Acid and Pectenotoxins in Individual Cells of Dinophysis and in Scallops Argopecten purpuratus from Perú

by Alex Alcántara-Rubira, Víctor Bárcena-Martínez, Maribel Reyes-Paulino, Katherine Medina-Acaro, Lilibeth Valiente-Terrones, Angélica Rodríguez-Velásquez, Rolando Estrada-Jiménez and Omar Flores-Salmón

Toxins 2018, 10(12), 490; https://doi.org/10.3390/toxins10120490 - 23 Nov 2018

Cited by 11 | Viewed by 4622

Abstract

Causative species of Harmful Algal Bloom (HAB) and toxins in commercially exploited molluscan shellfish species are monitored weekly from four classified shellfish production areas in Perú (three in the north and one in the south). Okadaic acid (OA) and pectenotoxins (PTXs) were detected [...] Read more.

Causative species of Harmful Algal Bloom (HAB) and toxins in commercially exploited molluscan shellfish species are monitored weekly from four classified shellfish production areas in Perú (three in the north and one in the south). Okadaic acid (OA) and pectenotoxins (PTXs) were detected in hand-picked cells of Dinophysis (D. acuminata-complex and D. caudata) and in scallops (Argopecten purpuratus), the most important commercial bivalve species in Perú. LC-MS analyses revealed two different toxin profiles associated with species of the D. acuminata-complex: (a) one with OA (0.3–8.0 pg cell⁻¹) and PTX2 (1.5–11.1 pg cell⁻¹) and (b) another with only PTX2 which included populations with different toxin cell quota (9.3–9.6 pg cell⁻¹ and 5.8–9.2 pg cell⁻¹). Toxin results suggest the likely presence of two morphotypes of the D. acuminata-complex in the north, and only one of them in the south. Likewise, shellfish toxin analyses revealed the presence of PTX2 in all samples (10.3–34.8 µg kg⁻¹), but OA (7.7–15.2 µg kg⁻¹) only in the northern samples. Toxin levels were below the regulatory limits established for diarrhetic shellfish poisoning (DSP) and PTXs (160 µg OA kg⁻¹) in Perú, in all samples analyzed. This is the first report confirming the presence of OA and PTX in Dinophysis cells and in shellfish from Peruvian coastal waters. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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14 pages, 2449 KiB

Open AccessArticle

Toxin Profiles of Okadaic Acid Analogues and Other Lipophilic Toxins in Dinophysis from Japanese Coastal Waters

by Hajime Uchida, Ryuichi Watanabe, Ryoji Matsushima, Hiroshi Oikawa, Satoshi Nagai, Takashi Kamiyama, Katsuhisa Baba, Akira Miyazono, Yuki Kosaka, Shinnosuke Kaga, Yukihiko Matsuyama and Toshiyuki Suzuki

Toxins 2018, 10(11), 457; https://doi.org/10.3390/toxins10110457 - 6 Nov 2018

Cited by 26 | Viewed by 4495

Abstract

The identification and quantification of okadaic acid (OA)/dinophysistoxin (DTX) analogues and pectenotoxins (PTXs) in Dinophysis samples collected from coastal locations around Japan were evaluated by liquid chromatography mass spectrometry. The species identified and analyzed included Dinophysis fortii, D. acuminata, D. mitra [...] Read more.

The identification and quantification of okadaic acid (OA)/dinophysistoxin (DTX) analogues and pectenotoxins (PTXs) in Dinophysis samples collected from coastal locations around Japan were evaluated by liquid chromatography mass spectrometry. The species identified and analyzed included Dinophysis fortii, D. acuminata, D. mitra (Phalacroma mitra), D. norvegica, D. infundibulus, D. tripos, D. caudata, D. rotundata (Phalacroma rotundatum), and D. rudgei. The dominant toxin found in D. acuminata was PTX2 although some samples contained DTX1 as a minor toxin. D. acuminata specimens isolated from the southwestern regions (Takada and Hiroshima) showed characteristic toxin profiles, with only OA detected in samples collected from Takada. In contrast, both OA and DTX1, in addition to a larger proportion of PTX2, were detected in D. acuminata from Hiroshima. D. fortii showed a toxin profile dominated by PTX2 although this species had higher levels of DTX1 than D. acuminata. OA was detected as a minor toxin in some D. fortii samples collected from Yakumo, Noheji, and Hakata. PTX2 was also the dominant toxin found among other Dinophysis species analyzed, such as D. norvegica, D. tripos, and D. caudata, although some pooled picked cells of these species contained trace levels of OA or DTX1. The results obtained in this study re-confirm that cellular toxin content and profiles are different even among strains of the same species. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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17 pages, 1607 KiB

Open AccessArticle

Diarrhetic Shellfish Toxin Monitoring in Commercial Wild Harvest Bivalve Shellfish in New South Wales, Australia

by Hazel Farrell, Penelope Ajani, Shauna Murray, Phil Baker, Grant Webster, Steve Brett and Anthony Zammit

Toxins 2018, 10(11), 446; https://doi.org/10.3390/toxins10110446 - 30 Oct 2018

Cited by 12 | Viewed by 4582

Abstract

An end-product market survey on biotoxins in commercial wild harvest shellfish (Plebidonax deltoides, Katelysia spp., Anadara granosa, Notocallista kingii) during three harvest seasons (2015–2017) from the coast of New South Wales, Australia found 99.38% of samples were within regulatory [...] Read more.

An end-product market survey on biotoxins in commercial wild harvest shellfish (Plebidonax deltoides, Katelysia spp., Anadara granosa, Notocallista kingii) during three harvest seasons (2015–2017) from the coast of New South Wales, Australia found 99.38% of samples were within regulatory limits. Diarrhetic shellfish toxins (DSTs) were present in 34.27% of 321 samples but only in pipis (P. deltoides), with two samples above the regulatory limit. Comparison of these market survey data to samples (phytoplankton in water and biotoxins in shellfish tissue) collected during the same period at wild harvest beaches demonstrated that, while elevated concentrations of Dinophysis were detected, a lag in detecting bloom events on two occasions meant that wild harvest shellfish with DSTs above the regulatory limit entered the marketplace. Concurrently, data (phytoplankton and biotoxin) from Sydney rock oyster (Saccostrea glomerata) harvest areas in estuaries adjacent to wild harvest beaches impacted by DSTs frequently showed elevated Dinophysis concentrations, but DSTs were not detected in oyster samples. These results highlighted a need for distinct management strategies for different shellfish species, particularly during Dinophysis bloom events. DSTs above the regulatory limit in pipis sampled from the marketplace suggested there is merit in looking at options to strengthen the current wild harvest biotoxin management strategies. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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21 pages, 3837 KiB

Open AccessArticle

Impact of Dinophysis acuminata Feeding Mesodinium rubrum on Nutrient Dynamics and Bacterial Composition in a Microcosm

by Han Gao, Chenfeng Hua and Mengmeng Tong

Toxins 2018, 10(11), 443; https://doi.org/10.3390/toxins10110443 - 30 Oct 2018

Cited by 10 | Viewed by 3634

Abstract

The development of Dinophysis populations, producers of diarrhetic shellfish toxins, has been attributed to both abiotic (e.g., water column stratification) and biotic (prey availability) factors. An important process to consider is mixotrophy of the Dinophysis species, which is an intensive feeding of the [...] Read more.

The development of Dinophysis populations, producers of diarrhetic shellfish toxins, has been attributed to both abiotic (e.g., water column stratification) and biotic (prey availability) factors. An important process to consider is mixotrophy of the Dinophysis species, which is an intensive feeding of the Mesodinium species for nutrients and a benefit from kleptochloroplasts. During the feeding process, the nutritional status in the environment changes due to the preference of Mesodinium and/or Dinophysis for different nutrients, prey cell debris generated by sloppy feeding, and their degradation by micro-organisms changes. However, there is little knowledge about the role of the bacterial community during the co-occurrence of Mesodinium and Dinophysis and how they directly or indirectly interact with the mixotrophs. In this study, laboratory experiments were performed to characterize the environmental changes including those of the prey present, the bacterial communities, and the ambient dissolved nutrients during the co-occurrence of Mesodinium rubrum and Dinophysis acuminata. The results showed that, during the incubation of the ciliate prey Mesodinium with its predator Dinophysis, available dissolved nitrogen significantly shifted from nitrate to ammonium especially when the population of M. rubrum decayed. Growth phases of Dinophysis and Mesodinium greatly affected the structure and composition of the bacterial community. These changes could be mainly explained by both the changes of the nutrient status and the activity of Dinophysis cells. Dinophysis feeding activity also accelerated the decline of M. rubrum and contamination of cultures with okadaic acid, dinophysistoxin-1, and pectenotoxin-2, but their influence on the prokaryotic communities was limited to the rare taxa (<0.1%) fraction. This suggests that the interaction between D. acuminata and bacteria is species-specific and takes place intracellularly or in the phycosphere. Moreover, a majority of the dominant bacterial taxa in our cultures may also exhibit a metabolic flexibility and, thus, be unaffected taxonomically by changes within the Mesodinium-Dinophysis culture system. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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26 pages, 2806 KiB

Open AccessArticle

RNA-Seq Analysis for Assessing the Early Response to DSP Toxins in Mytilus galloprovincialis Digestive Gland and Gill

by María Verónica Prego-Faraldo, Luisa Martínez and Josefina Méndez

Toxins 2018, 10(10), 417; https://doi.org/10.3390/toxins10100417 - 16 Oct 2018

Cited by 24 | Viewed by 4476

Abstract

The harmful effects of diarrhetic shellfish poisoning (DSP) toxins on mammalian cell lines have been widely assessed. Studies in bivalves suggest that mussels display a resistance to the cytogenotoxic effects of DSP toxins. Further, it seems that the bigger the exposure, the more [...] Read more.

The harmful effects of diarrhetic shellfish poisoning (DSP) toxins on mammalian cell lines have been widely assessed. Studies in bivalves suggest that mussels display a resistance to the cytogenotoxic effects of DSP toxins. Further, it seems that the bigger the exposure, the more resistant mussels become. To elucidate the early genetic response of mussels against these toxins, the digestive gland and the gill transcriptomes of Mytilus galloprovincialis after Prorocentrum lima exposure (100,000 cells/L, 48 h) were de novo assembled based on the sequencing of 8 cDNA libraries obtained using an Illumina HiSeq 2000 platform. The assembly provided 95,702 contigs. A total of 2286 and 4523 differentially expressed transcripts were obtained in the digestive gland and the gill, respectively, indicating tissue-specific transcriptome responses. These transcripts were annotated and functionally enriched, showing 44 and 60 significant Pfam families in the digestive gland and the gill, respectively. Quantitative PCR (qPCR) was performed to validate the differential expression patterns of several genes related to lipid and carbohydrate metabolism, energy production, genome integrity and defense, suggesting their participation in the protective mechanism. This work provides knowledge of the early response against DSP toxins in the mussel M. galloprovincialis and useful information for further research on the molecular mechanisms of the bivalve resistance to these toxins. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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20 pages, 3951 KiB

Open AccessArticle

Dinophysis acuta in Scottish Coastal Waters and Its Influence on Diarrhetic Shellfish Toxin Profiles

by Sarah C. Swan, Andrew D. Turner, Eileen Bresnan, Callum Whyte, Ruth F. Paterson, Sharon McNeill, Elaine Mitchell and Keith Davidson

Toxins 2018, 10(10), 399; https://doi.org/10.3390/toxins10100399 - 28 Sep 2018

Cited by 22 | Viewed by 4622

Abstract

Diarrhetic shellfish toxins produced by the dinoflagellate genus Dinophysis are a major problem for the shellfish industry worldwide. Separate species of the genus have been associated with the production of different analogues of the okadaic acid group of toxins. To evaluate the spatial [...] Read more.

Diarrhetic shellfish toxins produced by the dinoflagellate genus Dinophysis are a major problem for the shellfish industry worldwide. Separate species of the genus have been associated with the production of different analogues of the okadaic acid group of toxins. To evaluate the spatial and temporal variability of Dinophysis species and toxins in the important shellfish-harvesting region of the Scottish west coast, we analysed data collected from 1996 to 2017 in two contrasting locations: Loch Ewe and the Clyde Sea. Seasonal studies were also undertaken, in Loch Ewe in both 2001 and 2002, and in the Clyde in 2015. Dinophysis acuminata was present throughout the growing season during every year of the study, with blooms typically occurring between May and September at both locations. The appearance of D. acuta was interannually sporadic and, when present, was most abundant in the late summer and autumn. The Clyde field study in 2015 indicated the importance of a temperature front in the formation of a D. acuta bloom. A shift in toxin profiles of common mussels (Mytilus edulis) tested during regulatory monitoring was evident, with a proportional decrease in okadaic acid (OA) and dinophysistoxin-1 (DTX1) and an increase in dinophysistoxin-2 (DTX2) occurring when D. acuta became dominant. Routine enumeration of Dinophysis to species level could provide early warning of potential contamination of shellfish with DTX2 and thus determine the choice of the most suitable kit for effective end-product testing. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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15 pages, 2062 KiB

Open AccessArticle

Anatomical Distribution of Diarrhetic Shellfish Toxins (DSTs) in the Japanese Scallop Patinopecten yessoensis and Individual Variability in Scallops and Mytilus edulis Mussels: Statistical Considerations

by Ryoji Matsushima, Hajime Uchida, Ryuichi Watanabe, Hiroshi Oikawa, Izumi Oogida, Yuki Kosaka, Makoto Kanamori, Tatsuro Akamine and Toshiyuki Suzuki

Toxins 2018, 10(10), 395; https://doi.org/10.3390/toxins10100395 - 27 Sep 2018

Cited by 9 | Viewed by 3404

Abstract

Diarrhetic shellfish toxins (DSTs) are a group of phycotoxins that include okadaic acid (OA)/dinophysistoxin (DTX) analogues. At present, detailed data on the distribution of DST is insufficient, and studies of the appropriate sample sizes are lacking. This study investigated the DST frequency distribution [...] Read more.

Diarrhetic shellfish toxins (DSTs) are a group of phycotoxins that include okadaic acid (OA)/dinophysistoxin (DTX) analogues. At present, detailed data on the distribution of DST is insufficient, and studies of the appropriate sample sizes are lacking. This study investigated the DST frequency distribution in scallops and mussels by liquid chromatography-tandem mass spectrometry (LC/MS/MS) and a resampling analysis of existing data was carried out. The DST population-interval and the necessary sample size were also estimated. DSTs are localized in the scallop digestive-gland, and the DST concentrations in scallops were water-depth-dependent. DST concentrations in scallops and mussels showed normal distributions, but mussels tended to contain more DSTs than scallops. In the statistical resampling analysis of the acquired data on scallops and mussels, especially that using the bootstrap method, sample size was difficult to estimate when the DST variation was large. Although the DST population-interval could be statistically estimated from the sample standard deviation of three samples, the sample size corresponded to the risk management level, and the use of 13 or more samples was preferable. The statistical methods used here to analyze individual contents and estimate population content-intervals could be applied in various situations and for shellfish toxins other than DSTs. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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13 pages, 2573 KiB

Open AccessArticle

Accumulation and Biotransformation of Dinophysis Toxins by the Surf Clam Mesodesma donacium

by Juan Blanco, Gonzalo Álvarez, José Rengel, Rosario Díaz, Carmen Mariño, Helena Martín and Eduardo Uribe

Toxins 2018, 10(8), 314; https://doi.org/10.3390/toxins10080314 - 4 Aug 2018

Cited by 27 | Viewed by 4671

Abstract

Surf clams, Mesodesma donacium, were shown to accumulate toxins from Dinophysis acuminata blooms. Only pectenotoxin 2 (PTX2) and some of its derivatives were found, and no toxins from the okadaic acid group were detected. PTX2 seems to be transformed to PTX2 seco-acid [...] Read more.

Surf clams, Mesodesma donacium, were shown to accumulate toxins from Dinophysis acuminata blooms. Only pectenotoxin 2 (PTX2) and some of its derivatives were found, and no toxins from the okadaic acid group were detected. PTX2 seems to be transformed to PTX2 seco-acid (PTX2sa), which was found in concentrations more than ten-fold those of PTX2. The seco-acid was transformed to acyl-derivatives by esterification with different fatty acids. The estimated amount of these derivatives in the mollusks was much higher than that of PTX2. Most esters were originated by even carbon chain fatty acids, but some originated by odd carbon number were also found in noticeable concentrations. Some peaks of toxin in the bivalves did not coincide with those of Dinophysis abundance, suggesting that there were large differences in toxin content per cell among the populations that developed throughout the year. The observed depuration (from the digestive gland) was fast (more than 0.2 day⁻¹), and was faster for PTX2 than for PTX2sa, which in turn was faster than that of esters of PTX2sa. PTX2 and PTX2sa were distributed nearly equally between the digestive gland and the remaining tissues, but less than 5% of the palmytoyl-esters were found outside the digestive gland. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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17 pages, 4761 KiB

Open AccessArticle

Detoxification- and Immune-Related Transcriptomic Analysis of Gills from Bay Scallops (Argopecten irradians) in Response to Algal Toxin Okadaic Acid

by Cheng Chi, Sib Sankar Giri, Jin Woo Jun, Sang Wha Kim, Hyoun Joong Kim, Jeong Woo Kang and Se Chang Park

Toxins 2018, 10(8), 308; https://doi.org/10.3390/toxins10080308 - 28 Jul 2018

Cited by 30 | Viewed by 4682

Abstract

To reveal the molecular mechanisms triggered by okadaic acid (OA)-exposure in the detoxification and immune system of bay scallops, we studied differentially-expressed genes (DEGs) and the transcriptomic profile in bay scallop gill tissue after 48 h exposure to 500 nM of OA using [...] Read more.

To reveal the molecular mechanisms triggered by okadaic acid (OA)-exposure in the detoxification and immune system of bay scallops, we studied differentially-expressed genes (DEGs) and the transcriptomic profile in bay scallop gill tissue after 48 h exposure to 500 nM of OA using the Illumina HiSeq 4000 deep-sequencing platform. De novo assembly of paired-end reads yielded 55,876 unigenes, of which 3204 and 2620 genes were found to be significantly up- or down-regulated, respectively. Gene ontology classification and enrichment analysis of the DEGs detected in bay scallops exposed to OA revealed four ontologies with particularly high functional enrichment, which were ‘cellular process’ (cellular component), ‘metabolic process’ (biological process), ‘immune system process’ (biological process), and ‘catalytic process’ (molecular function). The DEGs revealed that cyclic AMP-responsive element-binding proteins, acid phosphatase, toll-like receptors, nuclear erythroid 2-related factor, and the NADPH2 quinone reductase-related gene were upregulated. In contrast, the expression of some genes related to glutathione S-transferase 1, C-type lectin, complement C1q tumor necrosis factor-related protein, Superoxide dismutase 2 and fibrinogen C domain-containing protein, decreased. The outcomes of this study will be a valuable resource for the study of gene expression induced by marine toxins, and will help understanding of the molecular mechanisms underlying the scallops’ response to OA exposure. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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13 pages, 1477 KiB

Open AccessArticle

Effect of Suspended Particulate Matter on the Accumulation of Dissolved Diarrhetic Shellfish Toxins by Mussels (Mytilus galloprovincialis) under Laboratory Conditions

by Aifeng Li, Meihui Li, Jiangbing Qiu, Jialiang Song, Ying Ji, Yang Hu, Shuqin Wang and Yijia Che

Toxins 2018, 10(7), 273; https://doi.org/10.3390/toxins10070273 - 3 Jul 2018

Cited by 24 | Viewed by 4028

Abstract

In recent years, detection of trace amounts of dissolved lipophilic phycotoxins in coastal waters has been possible using solid phase adsorption toxin tracking (SPATT) samplers. To explore the contribution of dissolved diarrhetic shellfish toxins (DST) to the accumulation of toxins by cultivated bivalves, [...] Read more.

In recent years, detection of trace amounts of dissolved lipophilic phycotoxins in coastal waters has been possible using solid phase adsorption toxin tracking (SPATT) samplers. To explore the contribution of dissolved diarrhetic shellfish toxins (DST) to the accumulation of toxins by cultivated bivalves, mussels (Mytilus galloprovincialis) were exposed to different concentrations of purified okadaic acid (OA) and dinophysistoxin-1 (DTX1) in filtered (0.45 µm) seawater for 96 h. Accumulation and esterification of DST by mussels under different experimental conditions, including with and without the addition of the food microalga Isochrysis galbana, and with the addition of different size-fractions of suspended particulate matter (SPM) (<75 µm, 75–150 µm, 150–250 µm) were compared. Results showed that mussels accumulated similar amounts of OA and DTX1 from seawater with or without food microalgae present, and slightly lower amounts when SPM particles were added. Mussels preferentially accumulated OA over DTX1 in all treatments. The efficiency of the mussel’s accumulation of OA and DTX1 from seawater spiked with low concentrations of toxins was higher than that in seawater with high toxin levels. A large proportion of OA (86–94%) and DTX1 (65–82%) was esterified to DTX3 by mussels in all treatments. The proportion of I. galbana cells cleared by mussels was markedly inhibited by dissolved OA and DTX1 (OA 9.2 µg L⁻¹, DTX1 13.2 µg L⁻¹) in seawater. Distribution of total OA and DTX1 accumulated in the mussel tissues ranked in all treatments as follows: digestive gland > gills > mantle > residual tissues. However, the percentage of total DST in the digestive gland of mussels in filtered seawater (67%) was higher than with the addition of SPM particles (75–150 µm) (51%), whereas the gills showed the opposite trend in filtered seawater with (27%) and without (14.4%) SPM particles. Results presented here will improve our understanding of the mechanisms of DST accumulation by bivalves in marine aquaculture environments. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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19 pages, 12528 KiB

Open AccessArticle

Diel Variations in Cell Abundance and Trophic Transfer of Diarrheic Toxins during a Massive Dinophysis Bloom in Southern Brazil

by Thiago Pereira Alves and Luiz Laureno Mafra, Jr.

Toxins 2018, 10(6), 232; https://doi.org/10.3390/toxins10060232 - 6 Jun 2018

Cited by 26 | Viewed by 4050

Abstract

Dinophysis spp. are a major source of diarrheic toxins to marine food webs, especially during blooms. This study documented the occurrence, in late May 2016, of a massive toxic bloom of the Dinophysis acuminata complex along the southern coast of Brazil, associated with [...] Read more.

Dinophysis spp. are a major source of diarrheic toxins to marine food webs, especially during blooms. This study documented the occurrence, in late May 2016, of a massive toxic bloom of the Dinophysis acuminata complex along the southern coast of Brazil, associated with an episode of marked salinity stratification. The study tracked the daily vertical distribution of Dinophysis spp. cells and their ciliate prey, Mesodinium cf. rubrum, and quantified the amount of lipophilic toxins present in seston and accumulated by various marine organisms in the food web. The abundance of the D. acuminata complex reached 43 × 10⁴ cells·L⁻¹ at 1.0 m depth at the peak of the bloom. Maximum cell densities of cryptophyceans and M. cf. rubrum (>500 × 10⁴ and 18 × 10⁴ cell·L⁻¹, respectively) were recorded on the first day of sampling, one week before the peak in abundance of the D. acuminata complex. The diarrheic toxin okadaic acid (OA) was the only toxin detected during the bloom, attaining unprecedented, high concentrations of up to 829 µg·L⁻¹ in seston, and 143 ± 93 pg·cell⁻¹ in individually picked cells of the D. acuminata complex. Suspension-feeders such as the mussel, Perna perna, and barnacle, Megabalanus tintinnabulum, accumulated maximum OA levels (up to 578.4 and 21.9 µg total OA·Kg⁻¹, respectively) during early bloom stages, whereas predators and detritivores such as Caprellidae amphipods (154.6 µg·Kg⁻¹), Stramonita haemastoma gastropods (111.6 µg·Kg⁻¹), Pilumnus spinosissimus crabs (33.4 µg·Kg⁻¹) and a commercially important species of shrimp, Xiphopenaeus kroyeri (7.2 µg·Kg⁻¹), only incorporated OA from mid- to late bloom stages. Conjugated forms of OA were dominant (>70%) in most organisms, except in blenny fish, Hypleurochilus fissicornis, and polychaetes, Pseudonereis palpata (up to 59.3 and 164.6 µg total OA·Kg⁻¹, respectively), which contained mostly free-OA throughout the bloom. Although algal toxins are only regulated in bivalves during toxic blooms in most countries, including Brazil, this study indicates that human seafood consumers might be exposed to moderate toxin levels from a variety of other vectors during intense toxic outbreaks. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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Review

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19 pages, 9709 KiB

Open AccessEditor’s ChoiceReview

Review of DSP Toxicity in Ireland: Long-Term Trend Impacts, Biodiversity and Toxin Profiles from a Monitoring Perspective

by Rafael Salas and Dave Clarke

Toxins 2019, 11(2), 61; https://doi.org/10.3390/toxins11020061 - 22 Jan 2019

Cited by 12 | Viewed by 5289

Abstract

The purpose of this work is to review all the historical monitoring data gathered by the Marine Institute, the national reference laboratory for marine biotoxins in Ireland, including all the biological and chemical data from 2005 to 2017, in relation to diarrheic shellfish [...] Read more.

The purpose of this work is to review all the historical monitoring data gathered by the Marine Institute, the national reference laboratory for marine biotoxins in Ireland, including all the biological and chemical data from 2005 to 2017, in relation to diarrheic shellfish poisoning (DSP) toxicity in shellfish production. The data reviewed comprises over 25,595 water samples, which were preserved in Lugol’s iodine and analysed for the abundance and composition of marine microalgae by light microscopy, and 18,166 records of shellfish flesh samples, which were analysed using LC-MS/MS for the presence and concentration of the compounds okadaic acid (OA), dinophysistoxins-1 (DTX-1), dinophysistoxins-2 (DTX-2) and their hydrolysed esters, as well as pectenotoxins (PTXs). The results of this review suggest that DSP toxicity events around the coast of Ireland occur annually. According to the data reviewed, there has not been an increase in the periodicity or intensity of such events during the study period. Although the diversity of the Dinophysis species on the coast of Ireland is large, with 10 species recorded, the two main species associated with DSP events in Ireland are D. acuta and D. acuminata. Moreover, the main toxic compounds associated with these species are OA and DTX-2, but concentrations of the hydrolysed esters are generally found in higher amounts than the parent compounds in the shellfish samples. When D. acuta is dominant in the water samples, the DSP toxicity increases in intensity, and DTX-2 becomes the prevalent toxin. Pectenotoxins have only been analysed and reported since 2012, and these compounds had not been associated with toxic events in Ireland; however, in 2014, concentrations of these compounds were quantitated for the first time, and the data suggest that this toxic event was associated with an unusually high number of observations of D. tripos that year. The areas of the country most affected by DSP outbreaks are those engaging in long-line mussel (Mytilus edulis) aquaculture. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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27 pages, 3315 KiB

Open AccessFeature PaperReview

Accumulation of Dinophysis Toxins in Bivalve Molluscs

by Juan Blanco

Toxins 2018, 10(11), 453; https://doi.org/10.3390/toxins10110453 - 2 Nov 2018

Cited by 56 | Viewed by 5877

Abstract

Several species of the dinoflagellate genus Dinophysis produce toxins that accumulate in bivalves when they feed on populations of these organisms. The accumulated toxins can lead to intoxication in consumers of the affected bivalves. The risk of intoxication depends on the amount and [...] Read more.

Several species of the dinoflagellate genus Dinophysis produce toxins that accumulate in bivalves when they feed on populations of these organisms. The accumulated toxins can lead to intoxication in consumers of the affected bivalves. The risk of intoxication depends on the amount and toxic power of accumulated toxins. In this review, current knowledge on the main processes involved in toxin accumulation were compiled, including the mechanisms and regulation of toxin acquisition, digestion, biotransformation, compartmentalization, and toxin depuration. Finally, accumulation kinetics, some models to describe it, and some implications were also considered. Full article

(This article belongs to the Special Issue Dinophysis Toxins: Distribution, Fate in Shellfish and Impacts)

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