Omic Technologies Applied to the Study of Marine Shellfish Toxins

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Marine and Freshwater Toxins".

Deadline for manuscript submissions: closed (15 April 2021) | Viewed by 20669

Special Issue Editors


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Guest Editor
Departamento de Bioquímica y Biología Molecular, Instituto de Acuicultura, Universidade de Santiago de Compostela, C/ Constantino Candeira, 15782 Santiago de Compostela, Spain.
Interests: marine shellfish toxins; toxin uptake and elimination in shellfish; biotransformation; gene expression; transcriptomics; bivalve mollusks; aquaculture; broodstock conditioning; metamorphosis

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Co-Guest Editor
Departamento de Bioquímica y Biología Molecular, Instituto de Acuicultura, Universidade de Santiago de Compostela, C/ Constantino Candeira, 15782 Santiago de Compostela, Spain.
Interests: marine shellfish toxins; toxin uptake and elimination in shellfish; molecular biology; transcriptomics; bivalve mollusks; aquaculture; broodstock conditioning; metamorphosis; settlement

Special Issue Information

Marine shellfish, especially filter feeders, can accumulate toxins in their tissues during harmful algal blooms. Toxins originated in phytoplankton species (dinoflagellates and diatoms principally) are ingested and are concentrated by shellfish. Consumption of toxin-containing shellfish can cause human health problems. The principal types of shellfish poisoning are paralytic (PSP), neurotoxic (NSP), diarrheic (DSP), amnestic (ASP) and azaspiracid (ASP). Shellfish toxins also have adverse economic impacts, leading to harvesting closures. The so called “-omics” technologies (genomics, transcriptomics, proteomics, and metabolomics) allow the simultaneous detection and quantification of thousands of genes, mRNAs, proteins or metabolites in a specific biological sample. These high-throughput technologies provide powerful methods to analyze all members of a family of molecules in a single analysis.

In this Special Issue, we welcome papers on all aspects of -omics approaches applied to the study of marine shellfish toxins. Topics of interest include but are not limited to: mechanisms of uptake, distribution, metabolism and excretion of toxins in shellfish; effects of toxins in shellfish at the molecular, cellular and physiological levels; identification of biomarkers that can be used to study toxin exposure and its effects; and molecular mechanisms of toxicity and identification of toxin metabolites.

Prof. Antonio J. Pazos
Prof. M. Luz Pérez-Parallé
Guest Editors

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Keywords

  • marine shellfish toxins
  • genomics
  • transcriptomics
  • proteomics
  • metabolomics
  • diarrheic shellfish poisoning
  • paralytic shellfish poisoning
  • amnesic shellfish poisoning
  • neurotoxic shellfish poisoning
  • harmful algal blooms

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Published Papers (6 papers)

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Research

20 pages, 3427 KiB  
Article
Expression Analyses of Genes Related to Multixenobiotic Resistance in Mytilus galloprovincialis after Exposure to Okadaic Acid-Producing Dinophysis acuminata
by Roi Martínez-Escauriaza, Vanessa Lozano, M. Luz Pérez-Parallé, Juan Blanco, José L. Sánchez and Antonio J. Pazos
Toxins 2021, 13(9), 614; https://doi.org/10.3390/toxins13090614 - 1 Sep 2021
Cited by 9 | Viewed by 2822
Abstract
The mussel Mytilus galloprovincialis is one of the most important aquaculture species in Europe. Its main production problem is the accumulation of toxins during coastal blooms, which prevents mussel commercialization. P-glycoprotein (ABCB1/MDR1/P-gp) is part of the multixenobiotic resistance system in aquatic organisms, and [...] Read more.
The mussel Mytilus galloprovincialis is one of the most important aquaculture species in Europe. Its main production problem is the accumulation of toxins during coastal blooms, which prevents mussel commercialization. P-glycoprotein (ABCB1/MDR1/P-gp) is part of the multixenobiotic resistance system in aquatic organisms, and okadaic acid, the main DSP toxin, is probably a substrate of the P-gp-mediated efflux. In this study, the presence and possible role of P-gp in the okadaic acid detoxification process was studied in M. galloprovincialis. We identified, cloned, and characterized two complete cDNAs of mdr1 and mdr2 genes. MgMDR1 and MgMDR2 predicted proteins had the structure organization of ABCB full transporters, and were identified as P-gp/MDR/ABCB proteins. Furthermore, the expression of mdr genes was monitored in gills, digestive gland, and mantle during a cycle of accumulation-elimination of okadaic acid. Mdr1 significantly increased its expression in the digestive gland and gills, supporting the idea of an important role of the MDR1 protein in okadaic acid efflux out of cells in these tissues. The expression of M. galloprovincialismrp2, a multidrug associated protein (MRP/ABCC), was also monitored. As in the case of mdr1, there was a significant induction in the expression of mrp2 in the digestive gland, as the content of okadaic acid increased. Thus, P-gp and MRP might constitute a functional defense network against xenobiotics, and might be involved in the resistance mechanisms to DSP toxins. Full article
(This article belongs to the Special Issue Omic Technologies Applied to the Study of Marine Shellfish Toxins)
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15 pages, 1358 KiB  
Article
Effect of Different Species of Prorocentrum Genus on the Japanese Oyster Crassostrea gigas Proteomic Profile
by Miguel Angel Matus Hernández and Norma Yolanda Hernández Saavedra
Toxins 2021, 13(7), 504; https://doi.org/10.3390/toxins13070504 - 20 Jul 2021
Cited by 1 | Viewed by 2692
Abstract
This paper assesses the effects of exposure to toxic concentrations (1200 to 6000 cells/mL) of the dinoflagellates Prorocentrum lima, Prorocentrum minimum, and Prorocentrum rhathymum and several concentrations of aqueous and organic extracts obtained from the same species (0 to 20 parts [...] Read more.
This paper assesses the effects of exposure to toxic concentrations (1200 to 6000 cells/mL) of the dinoflagellates Prorocentrum lima, Prorocentrum minimum, and Prorocentrum rhathymum and several concentrations of aqueous and organic extracts obtained from the same species (0 to 20 parts per thousand) on the Crassostrea gigas (5–7 mm) proteomic profile. Through comparative proteomic map analyses, several protein spots were detected with different expression levels, of which eight were selected to be identified by liquid chromatography–mass spectrometry (LC–MS/MS) analyses. The proteomic response suggests that, after 72 h of exposure to whole cells, the biological functions of C. gigas affected proteins in the immune system, stress response, contractile systems and cytoskeletal activities. The exposure to organic and aqueous extracts mainly showed effects on protein expressions in muscle contraction and cytoskeleton morphology. These results enrich the knowledge on early bivalve developmental stages. Therefore, they may be considered a solid base for new bioassays and/or generation of specific analytical tools that allow for some of the main effects of algal proliferation phenomena on bivalve mollusk development to be monitored, characterized and elucidated. Full article
(This article belongs to the Special Issue Omic Technologies Applied to the Study of Marine Shellfish Toxins)
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21 pages, 1896 KiB  
Article
Transcriptional Response in the Digestive Gland of the King Scallop (Pecten maximus) After the Injection of Domoic Acid
by Pablo Ventoso, Antonio J. Pazos, Juan Blanco, M. Luz Pérez-Parallé, Juan C. Triviño and José L. Sánchez
Toxins 2021, 13(5), 339; https://doi.org/10.3390/toxins13050339 - 7 May 2021
Cited by 10 | Viewed by 3522
Abstract
Some diatom species of the genus Pseudo-nitzschia produce the toxin domoic acid. The depuration rate of domoic acid in Pecten maximus is very low; for this reason, king scallops generally contain high levels of domoic acid in their tissues. A transcriptomic approach was [...] Read more.
Some diatom species of the genus Pseudo-nitzschia produce the toxin domoic acid. The depuration rate of domoic acid in Pecten maximus is very low; for this reason, king scallops generally contain high levels of domoic acid in their tissues. A transcriptomic approach was used to identify the genes differentially expressed in the P. maximus digestive gland after the injection of domoic acid. The differential expression analysis found 535 differentially expressed genes (226 up-regulated and 309 down-regulated). Protein–protein interaction networks obtained with the up-regulated genes were enriched in gene ontology terms, such as vesicle-mediated transport, response to stress, signal transduction, immune system process, RNA metabolic process, and autophagy, while networks obtained with the down-regulated genes were enriched in gene ontology terms, such as response to stress, immune system process, ribosome biogenesis, signal transduction, and mRNA processing. Genes that code for cytochrome P450 enzymes, glutathione S-transferase theta-1, glutamine synthase, pyrroline-5-carboxylate reductase 2, and sodium- and chloride-dependent glycine transporter 1 were among the up-regulated genes. Therefore, a stress response at the level of gene expression, that could be caused by the domoic acid injection, was evidenced by the alteration of several biological, cellular, and molecular processes. Full article
(This article belongs to the Special Issue Omic Technologies Applied to the Study of Marine Shellfish Toxins)
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14 pages, 3437 KiB  
Article
Tissue-Biased and Species-Specific Regulation of Glutathione Peroxidase (GPx) Genes in Scallops Exposed to Toxic Dinoflagellates
by Sein Moh Moh Hlaing, Jiarun Lou, Jie Cheng, Xiaogang Xun, Moli Li, Wei Lu, Xiaoli Hu and Zhenmin Bao
Toxins 2021, 13(1), 21; https://doi.org/10.3390/toxins13010021 - 31 Dec 2020
Cited by 12 | Viewed by 3068
Abstract
Marine bivalves could accumulate paralytic shellfish toxins (PSTs) produced by toxic microalgae, which might induce oxidative stress. Glutathione peroxidases (GPxs) are key enzymes functioning in the antioxidant defense, whereas our understanding of their roles in PST challenge in bivalves is limited. Herein, through [...] Read more.
Marine bivalves could accumulate paralytic shellfish toxins (PSTs) produced by toxic microalgae, which might induce oxidative stress. Glutathione peroxidases (GPxs) are key enzymes functioning in the antioxidant defense, whereas our understanding of their roles in PST challenge in bivalves is limited. Herein, through genome-wide screening, we identified nine (CfGPx) and eight (PyGPx) GPx genes in Zhikong scallop (Chlamys farreri) and Yesso scallop (Patinopecten yessoensis), respectively, and revealed the expansion of GPx3 sub-family in both species. RNA-Seq analysis revealed high expression of scallop GPx3s after D stage larva during early development, and in adult hepatopancreas. However, in scallops exposed to PST-producing dinoflagellates, no GPx was significantly induced in the hepatopancreas. In scallop kidneys where PSTs were transformed to higher toxic analogs, most CfGPxs were up-regulated, with CfGPx3s being acutely and chronically induced by Alexandrium minutum and A. catenella exposure, respectively, but only one PyGPx from GPx3 subfamily was up-regulated by A. catenella exposure. Our results suggest the function of scallop GPxs in protecting kidneys against the oxidative stresses by PST accumulation or transformation. The tissue-, species-, and toxin-dependent expression pattern of scallop GPxs also implied their functional diversity in response to toxin exposure. Full article
(This article belongs to the Special Issue Omic Technologies Applied to the Study of Marine Shellfish Toxins)
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22 pages, 2171 KiB  
Article
Differentiating Two Closely Related Alexandrium Species Using Comparative Quantitative Proteomics
by Bryan John J. Subong, Arturo O. Lluisma, Rhodora V. Azanza and Lilibeth A. Salvador-Reyes
Toxins 2021, 13(1), 7; https://doi.org/10.3390/toxins13010007 - 23 Dec 2020
Cited by 5 | Viewed by 4861
Abstract
Alexandrium minutum and Alexandrium tamutum are two closely related harmful algal bloom (HAB)-causing species with different toxicity. Using isobaric tags for relative and absolute quantitation (iTRAQ)-based quantitative proteomics and two-dimensional differential gel electrophoresis (2D-DIGE), a comprehensive characterization of the proteomes of A. minutum [...] Read more.
Alexandrium minutum and Alexandrium tamutum are two closely related harmful algal bloom (HAB)-causing species with different toxicity. Using isobaric tags for relative and absolute quantitation (iTRAQ)-based quantitative proteomics and two-dimensional differential gel electrophoresis (2D-DIGE), a comprehensive characterization of the proteomes of A. minutum and A. tamutum was performed to identify the cellular and molecular underpinnings for the dissimilarity between these two species. A total of 1436 proteins and 420 protein spots were identified using iTRAQ-based proteomics and 2D-DIGE, respectively. Both methods revealed little difference (10–12%) between the proteomes of A. minutum and A. tamutum, highlighting that these organisms follow similar cellular and biological processes at the exponential stage. Toxin biosynthetic enzymes were present in both organisms. However, the gonyautoxin-producing A. minutum showed higher levels of osmotic growth proteins, Zn-dependent alcohol dehydrogenase and type-I polyketide synthase compared to the non-toxic A. tamutum. Further, A. tamutum had increased S-adenosylmethionine transferase that may potentially have a negative feedback mechanism to toxin biosynthesis. The complementary proteomics approach provided insights into the biochemistry of these two closely related HAB-causing organisms. The identified proteins are potential biomarkers for organismal toxicity and could be explored for environmental monitoring. Full article
(This article belongs to the Special Issue Omic Technologies Applied to the Study of Marine Shellfish Toxins)
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14 pages, 1153 KiB  
Article
Differences in Toxic Response Induced by Three Variants of the Diarrheic Shellfish Poisoning Phycotoxins in Human Intestinal Epithelial Caco-2 Cells
by Antoine Huguet, Olivia Drapeau, Fanny Rousselet, Hélène Quenault and Valérie Fessard
Toxins 2020, 12(12), 783; https://doi.org/10.3390/toxins12120783 - 8 Dec 2020
Cited by 9 | Viewed by 2766
Abstract
Diarrheic shellfish poisoning (DSP) is caused by the consumption of shellfish contaminated with a group of phycotoxins that includes okadaic acid (OA), dinophysistoxin-1 (DTX-1), and dinophysistoxin-2 (DTX-2). These toxins are inhibitors of serine/threonine protein phosphatases 1 (PP1) and 2A (PP2A), but show distinct [...] Read more.
Diarrheic shellfish poisoning (DSP) is caused by the consumption of shellfish contaminated with a group of phycotoxins that includes okadaic acid (OA), dinophysistoxin-1 (DTX-1), and dinophysistoxin-2 (DTX-2). These toxins are inhibitors of serine/threonine protein phosphatases 1 (PP1) and 2A (PP2A), but show distinct levels of toxicity. Aside from a difference in protein phosphatases (PP) inhibition potency that would explain these differences in toxicity, others mechanisms of action are thought to be involved. Therefore, we investigated and compared which mechanisms are involved in the toxicity of these three analogues. As the intestine is one of the target organs, we studied the transcriptomic profiles of human intestinal epithelial Caco-2 cells exposed to OA, DTX-1, and DTX-2. The pathways specifically affected by each toxin treatment were further confirmed through the expression of key genes and markers of toxicity. Our results did not identify any distinct biological mechanism for OA and DTX-2. However, only DTX-1 induced up-regulation of the MAPK transduction signalling pathway, and down-regulation of gene products involved in the regulation of DNA repair. As a consequence, based on transcriptomic results, we demonstrated that the higher toxicity of DTX-1 compared to OA and DTX-2 was consistent with certain specific pathways involved in intestinal cell response. Full article
(This article belongs to the Special Issue Omic Technologies Applied to the Study of Marine Shellfish Toxins)
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