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Marine Biotoxins and Seafood Poisoning Marine Biotoxins and Seafood Poisoning Edited by Pedro Reis Costa, Jorge Diogène and Antonio Marques Printed Edition of the Special Issue Published in Toxins www.mdpi.com/journal/toxins Marine Biotoxins and Seafood Poisoning Marine Biotoxins and Seafood Poisoning Special Issue Editors Pedro Reis Costa Jorge Diog`ene Antonio Marques MDPI • Basel • Beijing • Wuhan • Barcelona • Belgrade Special Issue Editors Pedro Reis Costa Jorge Diogene` IPMA IRTA Portugal Spain Antonio Marques IPMA Portugal Editorial Office MDPI St. Alban-Anlage 66 4052 Basel, Switzerland This is a reprint of articles from the Special Issue published online in the open access journal Toxins (ISSN 2072-6651) from 2018 to 2019 (available at: https://www.mdpi.com/journal/toxins/special issues/Biotoxin Seafood) For citation purposes, cite each article independently as indicated on the article page online and as indicated below: LastName, A.A.; LastName, B.B.; LastName, C.C. Article Title. Journal Name Year, Article Number, Page Range. ISBN 978-3-03921-818-9 (Pbk) ISBN 978-3-03921-819-6 (PDF) c 2019 by the authors. Articles in this book are Open Access and distributed under the Creative Commons Attribution (CC BY) license, which allows users to download, copy and build upon published articles, as long as the author and publisher are properly credited, which ensures maximum dissemination and a wider impact of our publications. The book as a whole is distributed by MDPI under the terms and conditions of the Creative Commons license CC BY-NC-ND. Contents About the Special Issue Editors ..................................... vii Pedro Reis Costa, Ant´onio Marques and Jorge Diog`ene Marine Biotoxins and Seafood Poisoning Reprinted from: Toxins 2019, 11, 558, doi:10.3390/toxins11100558 .................. 1 John Kristoffer Andres, Aletta T. Yniguez, ˜ Jennifer Mary Maister, Andrew D. Turner, Dave Eldon B. Olano, Jenelyn Mendoza, Lilibeth Salvador-Reyes and Rhodora V. Azanza Paralytic Shellfish Toxin Uptake, Assimilation, Depuration, and Transformation in the Southeast Asian Green-Lipped Mussel (Perna viridis) Reprinted from: Toxins 2019, 11, 468, doi:10.3390/toxins11080468 .................. 3 Vera Barbosa, Marta Santos, Patr´ıcia Anacleto, Ana Lu´ısa Maulvault, Pedro Pous˜ao-Ferreira, Pedro Reis Costa and Ant´onio Marques Paralytic Shellfish Toxins and Ocean Warming: Bioaccumulation and Ecotoxicological Responses in Juvenile Gilthead Seabream (Sparus aurata) Reprinted from: Toxins 2019, 11, 408, doi:10.3390/toxins11070408 .................. 16 Kathi A. Lefebvre, Betsy Jean Yakes, Elizabeth Frame, Preston Kendrick, Sara Shum, Nina Isoherranen, Bridget E. Ferriss, Alison Robertson, Alicia Hendrix, David J. Marcinek and Lynn Grattan Discovery of a Potential Human Serum Biomarker for Chronic Seafood Toxin Exposure Using an SPR Biosensor Reprinted from: Toxins 2019, 11, 293, doi:10.3390/toxins11050293 .................. 32 Manabu Asakawa, Takuya Matsumoto, Kohei Umezaki, Kyoichiro Kaneko, Ximiao Yu, Gloria Gomez-Delan, Satoshi Tomano, Tamao Noguchi and Susumu Ohtsuka Toxicity and Toxin Composition of the Greater Blue-Ringed Octopus Hapalochlaena lunulata from Ishigaki Island, Okinawa Prefecture, Japan Reprinted from: Toxins 2019, 11, 245, doi:10.3390/toxins11050245 .................. 47 Gonzalo Alvarez,´ Patricio A. D´ıaz, Marcos Godoy, Michael Araya, Iranzu Ganuza, Roberto Pino, Francisco Alvarez,´ Jos´e Rengel, Cristina Hern´andez, Eduardo Uribe and Juan Blanco Paralytic Shellfish Toxins in Surf Clams Mesodesma donacium during a Large Bloom of Alexandrium catenella Dinoflagellates Associated to an Intense Shellfish Mass Mortality Reprinted from: Toxins 2019, 11, 188, doi:10.3390/toxins11040188 .................. 56 Si Chen, Xiaojun Zhang, Zhongyong Yan, Yangyang Hu and Yibo Lu Development and Application of Immunoaffinity Column Purification and Ultrahigh Performance Liquid Chromatography-Tandem Mass Spectrometry for Determination of Domoic Acid in Shellfish Reprinted from: Toxins 2019, 11, 83, doi:10.3390/toxins11020083 ................... 74 Aiko Hayashi, Juan Jos´e Dorantes-Aranda, John P. Bowman and Gustaaf Hallegraeff Combined Cytotoxicity of the Phycotoxin Okadaic Acid and Mycotoxins on Intestinal and Neuroblastoma Human Cell Models Reprinted from: Toxins 2018, 10, 526, doi:10.3390/toxins10120526 .................. 90 v About the Special Issue Editors Pedro Reis Costa received his PhD degree in Marine Biology and Ecology from the University of Lisbon (Portugal, 2006), and continued as a Postdoctoral Fellow in NOAA Fisheries Science Center (Seattle, USA) in 2007–2009. He has been a Researcher at the Portuguese Institute of the Sea and Atmosphere (IPMA) since his appointment in 2009. He is mainly interested in the study of harmful algal blooms (HAB) and the transfer of marine toxins in the food web, including their fate and toxicological potential in marine/estuarine environments. Jorge Diog`ene graduated in Biology at the Universitat de Barcelona (Spain, 1985) and holds an MSc in Marine Biology (University of South Alabama, USA, 1988) and PhD in Toxicology from the Universite´ Paris 7 (France, 1993). He is Head of both the Unitat de Seguiment del Medi and the Marine and Continental Waters program at IRTA-Sant Carles de la Rapita.` His research interests are oriented towards the evaluation of toxin production of microalgae, toxin determination in shellfish, and the development of cell-based assays used to identify and quantify the toxicological potential of toxins. His responsibilities focus on the monitoring program for the quality of water in shellfish harvesting areas, as well as in the field of seafood quality analysis and food safety evaluation. Antonio Marques received his PhD degree in Applied Biological Sciences from the University of Ghent (Belgium, 2005) and continued as a Researcher at the Portuguese Institute of the Sea and Atmosphere (IPMA) in 2006–2015. He has been a Senior Researcher at IPMA since his appointment in 2015. His main interests are in seafood quality and safety (chemical contaminants), innovative solutions for the seafood production and processing industries, seafood preservation methodologies, and climate change. vii toxins Editorial Marine Biotoxins and Seafood Poisoning Pedro Reis Costa 1, António Marques 1 and Jorge Diogène 2,* 1 IPMA-Portuguese Institute for the Sea and Atmosphere, Av. Alfredo Magalhães Ramalho 6, 1495-165 Lisbon, Portugal; [email protected] (P.R.C.); [email protected] (A.M.) 2 IRTA Institute of Agrifood Research and Technology, IRTA, Ctra. Villafranco, 5, 43540 Sant Carles de la Ràpita, Spain * Correspondence: [email protected] Received: 9 September 2019; Accepted: 17 September 2019; Published: 24 September 2019 Prevalence of marine biotoxins in seafood has been associated with increasing frequency, intensity, and duration of harmful algal blooms, and an increase of the geographical and temporal distribution of harmful algae. New and emerging biotoxins have been recurrently detected in regions where they were previously absent, raising challenges to the economic sustainability of seafood production in coastal areas and to consumer health safety. The economic burden to seafood producers caused by the closure of production areas and a possible feeling of insecurity from consumers urges researchers to improve available knowledge on toxin dynamics in marine organisms and the environment. Epidemiological studies are scarce and risk characterization is needed, particularly for emerging toxins. It is critical to enhance collaborative multi- and trans-disciplinary actions to introduce eco-innovative sustainable strategies to improve shellfish and fish safety. Strengthening industrial competitiveness is achievable by developing fast and reliable methods for marine biotoxin detection, and by implementing mitigation strategies. Innovative toxicological approaches for seafood safety evaluation are also required. The seven articles of this special issue address such research needs and are organized into three groups: (i) toxin dynamics and effects in marine organisms, (ii) development of detection methods for marine toxins, and (iii) toxin exposure and risks associated with the consumption of contaminated seafood. Within the first group of articles, Alvarez et al. [1] reported an extreme event in southern Chile of a bloom of Alexandrium catenella that caused mass mortality of several marine invertebrate species, and resulted in accumulation of high levels (exceeding 100 times the regulatory limit for human consumption) of paralytic shellfish poisoning (PSP) toxins in clams. This study highlights the need for assessing toxin dynamics in shellfish under controlled conditions to better understand and foresee the impacts of harmful algal blooms. Andres et al. [2] fed green-lipped mussel (Perna viridis) with the toxic dinoflagellate Alexandrium minutum under controlled laboratory conditions to assess the dynamics of PSP toxin levels during accumulation and elimination phases. Barbosa et al. [3] investigated the interaction of ocean warming with fish (Sparus aurata) exposure to PSP toxins through contaminated mussels to assess physiological responses and changes in toxin accumulation. Tetrodotoxin (TTX), which has a mode of action comparable to PSP toxins, was characterized in the greater blue-ringed octopus Hapalochlaena lunulata from Okinawa, Japan [4]. Regarding the development and optimization of methods for toxin detection, Chen and colleagues [5] optimized clean-up procedures based on immunoaffinity column purification before mass spectrometry
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