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- Toxin profile of Ostreopsis cf. ovata from Portuguese continental coast and Selvagens Islands (Madeira, Portugal)Publication . Soliño, Lucia; Garcia-Altares, Maria; Godinho, Lia; Reis Costa, PedroThe toxigenic dinoflagellate Ostreopsis cf. ovata is known to produce a range of palytoxin (PLTX) - related compounds named ovatoxins (OVTX). O. cf. ovata presents a wide variability in toxin production and its toxic profile is strain-specific. Several OVTXs, denominated from -a to -h and -I have been reported from different strains of this benthic microalgae up to now, mainly in Mediterranean isolates. However, less is known about the toxin profile of the strains present in the Atlantic coasts of Europe. In this work, strains of O. cf. ovata isolated from the South coast of Portugal mainland (Algarve) and Selvagens Island (Madeira, Portugal) were cultured and tested for toxicity by hemolytic assay. Toxin profiles were qualitatively elucidated by Liquid Chromatography-High Resolution Mass Spectrometry (LC-HRMS). The strain from Algarve presented lower toxic potency than the strain from Selvagens island (12.3 against 54.8 pg of PLTX equivalents per cell) showing in both cases the characteristic toxin profile of Mediterranean strains. The major component, OVTX-a, was concomitant with OVTX from -b to -g and isobaric PLTX. Regarding the morphological characteristics of these strains, as well as their toxin fingerprint, it is likely they are closely related to strains from Mediterranean coasts. The present study reports for the first time the occurrence of several OVTX congeners and iso-PLTX in O. cf. ovata from Portuguese waters. This study provides valuable information to characterize the risk of OVTXs-related outbreaks in Portugal.
- New insights into the occurrence of paralytic shellfish toxins in the oceanic pufferfish Lagocephalus lagocephalus (Linnaeus, 1758) from Madeira Island, PortugalPublication . Soliño, Lucia; Gouveia, Neide; Timóteo, Viriato; Reis Costa, PedroPufferfish are some of the most poisonous marine organisms due to their capability to accumulate potent neurotoxins such as tetrodotoxins (TTXs) and paralytic shellfish toxins (PSTs). Several species are consumed, mainly in Asiatic countries, for the quality of their flesh, which may cause severe human poisoning every year due to errors in preparation. Lagocephalus lagocephalus the oceanic pufferfish, is a cosmopolitan species present in European Atlantic and Mediterranean coasts. Although considered toxic, only a few studies have previously addressed the occurrence of toxic compounds in this species. In the present study, 29 individuals of L. lagocephalus caught in Madeira Island (NE Atlantic) were dissected and analysed by HPLC-FLD for PSTs detection. Saxitoxin (STX) and decarbamoyl STX (dcSTX) were detected in liver, intestine and gonads but not in the muscle. Neosaxitoxin (NEO) could also be detected in a liver sample. The total STX equivalent (eq) concentrations in liver ranged from < LOQ to 973.4 μg STX eq kg−1. The presence of toxins in the intestines and gonads points to the fish capability to acquire toxins through feeding or by association with endosymbiotic, toxin-producing microbes as well as the ability to accumulate them in specific organs. Although pufferfish trade in Europe is forbidden by European Union regulations, the increasing occurrence of this species in new areas and the expected raise of blooms of PSTs-producer organisms claims for a better knowledge on oceanic pufferfish toxicity and biology. This will be needed to provide accurate information to stakeholders and population to prevent illegal trade of these species and poisoning incidents.
- Distribution, identification and cytotoxicity of Gambierdiscus (Dinophyceae) in the Atlantic Selvagens Islands (Madeira, Portugal): a ciguatera gateway to EuropePublication . Godinho, Lia; Soliño, Lucia; Churro, Catarina; Timoteo, Viriato; Santos, Carolina; Gouveia, Neide; Diogène, Jorge; Reis Costa, PedroThe emerging threat of ciguatera poisoning (CP) in Europe has been associated with fish captured in the Canary Islands (Spain) and Selvagens Islands (Portugal). The first are heavily populated islands where numerous scientific studies have been carried out. Conversely, the Selvagens Islands are a nature reserve with low human pressure that have been rarely surveyed in terms of the marine benthic microalgae, including the epiphytic ciguatera-causing dinoflagellate species. To investigate the harmful microalgal diversity of the Selvagens Islands, a scientific cruise to these remote islands took place in September, 2018. The Gambierdiscus species composition and distribution, and the associated epiphytic dinoflagellate community, were assessed using artificial substrate devices. Gambierdiscus cells were found in all samples, reaching concentrations of up to 725 cells 100 cm(-2). G. australes was the only species identified after morphological and molecular analysis of the retrieved cultures. Species identification was confirmed by molecular characterization based on the LSU D8-D10 region. Nevertheless, phylogenetic studies indicated that some strains diverged from the G. australes clade suggesting genetic differentiation. Toxicity was estimated by neuro-2a cell-based assay in four strains, ranging from 2.46-83 fg of CTX1B eq. cell(-1). The epiphytic dinoflagellate community that co-occurred with Gambierdiscus comprised other toxic or potentially toxic dinoflagellates, such as Ostreopsis, Prorocentrum, Amphidinium and Coolia species. Oceanographic and meteorological data were also obtained to characterize the occurrence of Gambierdiscus. This study is the first stage in understanding the role of the Selvagens Islands in the incubation and proliferation of the ciguatera-causing dinoflagellates Gambierdiscus in the NE Atlantic.
- LC-HRMS profiling of paralytic shellfish toxins in Mytilus galloprovincialis after a Gymnodinium catenatum bloomPublication . Lage, Sandra; Reis Costa, Pedro; Canario, Adelino; Da Silva, José PauloSaxitoxin and its more than 50 analogues are a group of naturally occurring neurotoxins collectively designated as paralytic shellfish toxins (PSTs). PSTs are toxic to humans and maximum legal limits in seafood have been implemented by regulatory authorities worldwide. In the European Union, monitoring of PSTs is performed using the AOAC Official Method 2005.06, based on liquid chromatography coupled with fluorescence detection (LC- FLD). However, this method has been suggested to not effectively detect the emerging C-11 hydroxyl (M-toxins) and benzoate (GC-toxins) analogues, with these analogues currently not being surveyed in monitoring programs. In this study, a liquid chromatography-high resolution mass spectrometry (LC-HRMS) method was used to search for these emerging PSTs in mussels, Mytilus galloprovincialis, contaminated following an intense Gymnodinium catenatum bloom in the Tagus estuary (Lisbon, Portugal). Five M-toxins (M1, M2, M6, dcM6, and dcM10), but no GC-toxins, were detected in the mussels’ whole-soft body tissue. Moreover, the classical PSTs (C1 to C4, GTX 4 to GTX6, dcGTX1 to dcGTX4, dcSTX, dcNEO, and STX) were also found and comprised the largest fraction of the PSTs’ profile. The presence of unregulated PSTs in edible mussel samples suggests potential seafood safety risks and urges further research to determine the frequency of these analogues in seafood and their contribution to toxicity
- Quantitation overcoming Matrix effects of Lipophilic toxins in Mytilus galloprovincialis by liquid chromatography-full scan high resolution mass spectrometry analysis (LC-HR-MS)Publication . Costa, Camila Q. V. da; Afonso, Inês I.; Lage, Sandra; Costa, Pedro Reis; Canario, Adelino; Silva, José Paulo daThe analysis of marine lipophilic toxins in shellfish products still represents a challenging task due to the complexity and diversity of the sample matrix. Liquid chromatography coupled with mass spectrometry (LC-MS) is the technique of choice for accurate quantitative measurements in complex samples. By combining unambiguous identification with the high selectivity of tandem MS, it provides the required high sensitivity and specificity. However, LC-MS is prone to matrix effects (ME) that need to be evaluated during the development and validation of methods. Furthermore, the large sample-to-sample variability, even between samples of the same species and geographic origin, needs a procedure to evaluate and control ME continuously. Here, we analyzed the toxins okadaic acid (OA), dinophysistoxins (DTX-1 and DTX-2), pectenotoxin (PTX-2), yessotoxin (YTX) and azaspiracid-1 (AZA-1). Samples were mussels (Mytilus galloprovincialis), both fresh and processed, and a toxin-free mussel reference material. We developed an accurate mass-extracted ion chromatogram (AM-XIC) based quantitation method using an Orbitrap instrument, evaluated the ME for different types and extracts of mussel samples, characterized the main compounds co-eluting with the targeted molecules and quantified toxins in samples by following a standard addition method (SAM). An AM-XIC based quantitation of lipophilic toxins in mussel samples using high resolution and accuracy full scan profiles (LC-HR-MS) is a good alternative to multi reaction monitoring (MRM) for instruments with HR capabilities. ME depend on the starting sample matrix and the sample preparation. ME are particularly strong for OA and related toxins, showing values below 50% for fresh mussel samples. Results for other toxins (AZA-1, YTX and PTX-2) are between 75% and 110%. ME in unknown matrices can be evaluated by comparing their full scan LC-HR-MS profiles with those of known samples with known ME. ME can be corrected by following SAM with AM-XIC quantitation if necessary.
- Bivalve shellfish safety in Portugal: variability of faecal levels, metal contaminants and marine biotoxins during the last decade (2011–2020)Publication . Braga, Ana Catarina; Rodrigues, Susana Margarida; Lourenço, Helena Maria; Reis Costa, Pedro; Pedro, SóniaBivalves are a high-value product whose production has markedly increased, reaching 9863 tonnes in Portugal in 2021. Bivalves' habitats-lagoons, estuaries and coastal waters-are exposed to biological and anthropogenic contaminants, which can bioaccumulate in these organisms and pose a significant public health risk. The need to obtain a safe product for human consumption led to the implementation of standardised hygiene regulations for harvesting and marketing bivalve molluscs, resulting in routine monitoring of bivalve production areas for microbial quality, metal contaminants, and marine biotoxins. While excessive levels of biotoxins and metal contamination lead to temporary harvesting bans, high faecal contamination leads to area reclassification and impose post-harvest treatments. In this study, the seasonal and temporal variability of these parameters were analysed using historical data generated by the monitoring programme during the last decade. Moreover, the impact of the monitoring program on bivalve harvesting from 2011 to 2020 was assessed. This program presented a considerable improvement over time, with an increase in the sampling effort and the overall program representativeness. Finally, contamination risk, revising control measures, and defining recommendations for risk mitigation measures are given in the light of ten years' monitoring.
- Projecting future climate change-mediated impacts in Three Paralytic Shellfish Toxins-Producing dinoflagellate speciesPublication . Borges, Francisco O.; Lopes, Vanessa M.; Amorim, Ana; Santos, Catarina F.; Reis Costa, Pedro; Rosa, RuiSimple Summary Harmful algal blooms present a particular risk for marine ecosystems and human health alike. In this sense, it is important to accurately predict how toxin-producing microalgae could be affected by future climate change. The present study applied species distribution models (SDMs) to project the potential changes in the habitat suitability and distribution of three key paralytic shellfish toxin (PST)-producing dinoflagellate species (i.e., Alexandrium catenella, A. minutum, and Gymnodinium catenatum), up to 2040/50 and 2090/2100, across four different greenhouse gas emission scenarios, and using four abiotic predictors (i.e., sea surface temperature, salinity, current velocity, and bathymetry). In general, considerable contractions were observed for all three species in the lower latitudes of their distribution, together with projected expansions into higher latitudes, particularly in the Northern Hemisphere. This study aims to entice further research on the future biogeographical impacts of climate change in toxin-producing microalgae species while, at the same time, helping to advise the correct environmental management of coastal habitats and ecosystems. Toxin-producing microalgae present a significant environmental risk for ecosystems and human societies when they reach concentrations that affect other aquatic organisms or human health. Harmful algal blooms (HAB) have been linked to mass wildlife die-offs and human food poisoning episodes, and climate change has the potential to alter the frequency, magnitude, and geographical extent of such events. Thus, a framework of species distribution models (SDMs), employing MaxEnt modeling, was used to project changes in habitat suitability and distribution of three key paralytic shellfish toxin (PST)-producing dinoflagellate species (i.e., Alexandrium catenella, A. minutum, and Gymnodinium catenatum), up to 2050 and 2100, across four representative concentration pathway scenarios (RCP-2.6, 4.5, 6.0, and 8.5; CMIP5). Despite slightly different responses at the regional level, the global habitat suitability has decreased for all the species, leading to an overall contraction in their tropical and sub-tropical ranges, while considerable expansions are projected in higher latitudes, particularly in the Northern Hemisphere, suggesting poleward distributional shifts. Such trends were exacerbated with increasing RCP severity. Yet, further research is required, with a greater assemblage of environmental predictors and improved occurrence datasets, to gain a more holistic understanding of the potential impacts of climate change on PST-producing species.
- Impacts of climate change on the biogeography of three amnesic shellfish toxin producing diatom speciesPublication . Borges, Francisco O.; Lopes, Vanessa M.; Santos, Catarina Frazão; Reis Costa, Pedro; Rosa, RuiHarmful algal blooms (HABs) are considered one of the main risks for marine ecosystems and human health worldwide. Climate change is projected to induce significant changes in species geographic distribution, and, in this sense, it is paramount to accurately predict how it will affect toxin-producing microalgae. In this context, the present study was intended to project the potential biogeographical changes in habitat suitability and occurrence distribution of three key amnesic shellfish toxin (AST)-producing diatom species (i.e., Pseudo-nitzschia australis, P. seriata, and P. fraudulenta) under four different climate change scenarios (i.e., RCP-2.6, 4.5, 6.0, and 8.5) up to 2050 and 2100. For this purpose, we applied species distribution models (SDMs) using four abiotic predictors (i.e., sea surface temperature, salinity, current velocity, and bathymetry) in a MaxEnt framework. Overall, considerable contraction and potential extirpation were projected for all species at lower latitudes together with projected poleward expansions into higher latitudes, mainly in the northern hemisphere. The present study aims to contribute to the knowledge on the impacts of climate change on the biogeography of toxin-producing mi
- In vitro bioaccessibility of the marine biotoxins okadaic acid, dinophysistoxin-2 and their 7-O-acyl fatty acid ester derivatives in raw and steamed shellfishPublication . Manita, Diana; Alves, Ricardo N.; Braga, Ana Catarina; Fogaca, Fabiola H. S.; Marques, Antonio; Reis Costa, PedroOkadaic acid (OA), Dinophysistoxins (DTX1 and DTX2) and their acyl-derivatives (DTX3) are marine toxins responsible for the human diarrhetic shellfish poisoning. To date the amount of toxins ingested from consumption of shellfish has been considered equal to the amount of toxins available for uptake by the human body. The aim of this study is to assess the OA, DTX2 and DTX3 fractions released from raw and steamed mussels and cockles into the digestive fluids (bioaccessibility) using a static in vitro digestion model. Higher bioaccessibility was found in mussels (86 +/- 4%) than in cockles (59 +/- 9%). A significant reduction of ester derivatives of OA and an increase of OA were observed in the bioaccessible fraction of mussel samples, suggesting that DTX3 undergo conversion into their more toxic parent compounds during human digestion. However, similar increase of DTX2 and reduction of the respective acyl derivatives was not observed. Steaming lead to significant reduction of OA and analogues bioaccessibility in both species even though increased concentrations of toxins are obtained after this treatment. Risk assessment based solely on DSP toxins occurrence in seafood can conduct to an overestimation of the exposure and lead to more conservative regulatory measures. (C) 2017 Elsevier Ltd. All rights reserved.
- Global impact of ciguatoxins and ciguatera fish poisoning on fish, fisheries and consumersPublication . Soliño, Lucia; Reis Costa, PedroCiguatera fish poisoning (CFP) is one of the most devastating food-borne illnesses caused by fish consumption. Ciguatoxins (CTXs) are potent neurotoxins synthesized by the benthic microalgae Gambierdiscus spp. and Fukuyoa spp. that are transmitted to fish by grazing and predation. Despite the high incidence of CFP, affecting an estimated number of 50,000 persons per year in tropical and subtropical latitudes, the factors underlying CTXs occurrence are still not well understood. Toxin transfer and dynamics in fish and food-webs are complex. Feeding habits and metabolic pathways determine the toxin profile and toxicity of fish, and migratory species may transport and spread the hazard. Furthermore, CTX effect on fish may be a limiting factor for fish recruitment and toxin prevalence. Recently, new occurrences of Gambierdiscus spp. in temperate areas have been concomitant with the detection of toxic fish and CFP incidents in non-endemic areas. CFP cases in Europe have led to implementation of monitoring programs and fisheries restrictions with considerable impact on local economies. More than 400 species of fish can be vectors of CTXs, and most of them are high-valued commercial species. Thus, the risk uncertainty and the spread of Gambierdiscus have serious consequences for fisheries and food safety. Here, we present a critical review of CTXs impacts on fish, fisheries, and humans, based on the current knowledge on CFP incidence and CTXs prevalence in microalgae and fish.