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Emerging Marine Biotoxins Emerging Marine Biotoxins Edited by Ana Gago-Martínez and Arjen Gerssen Printed Edition of the Special Issue Published in Toxins www.mdpi.com/journal/toxins Emerging Marine Biotoxins Emerging Marine Biotoxins Special Issue Editors Ana Gago-Mart´ınez Arjen Gerssen MDPI • Basel • Beijing • Wuhan • Barcelona • Belgrade Special Issue Editors Ana Gago-Mart´ınez Arjen Gerssen Universidad de Vigo Wageningen University and Research Spain The Netherlands 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/Emerging marine biotoxins) 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 978-3-03921-349-8 (Pbk) ISBN 978-3-03921-513-3 (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 Arjen Gerssen and Ana Gago-Mart´ınez Emerging Marine Biotoxins Reprinted from: Toxins 2019, 11, 314, doi:10.3390/toxins11060314 .................. 1 Pablo Estevez, David Castro, Ana Peque ˜no-Valtierra, Jos´eM. Leao, Oscar Vilarino, ˜ Jorge Diog`eneand Ana Gago-Mart´ınez An Attempt to Characterize the Ciguatoxin Profile in Seriola fasciata Causing Ciguatera Fish Poisoning in Macaronesia Reprinted from: Toxins 2019, 11, 221, doi:10.3390/toxins11040221 .................. 4 Pedro Reis Costa, Pablo Estevez, David Castro, Luc´ıa Soli ˜no,Neide Gouveia, Carolina Santos, Susana Margarida Rodrigues, Jos´eManuel Leao and Ana Gago-Mart´ınez New Insights into the Occurrence and Toxin Profile of Ciguatoxins in Selvagens Islands (Madeira, Portugal) Reprinted from: Toxins 2018, 10, 524, doi:10.3390/toxins10120524 .................. 17 Bo Wang, Mimi Yao, Jin Zhou, Shangjin Tan, Hui Jin, Feng Zhang, Yim Ling Mak, Jiajun Wu, Leo Lai Chan and Zhonghua Cai Growth and Toxin Production of Gambierdiscus spp. Can Be Regulated by Quorum-Sensing Bacteria Reprinted from: Toxins 2018, 10, 257, doi:10.3390/toxins10070257 .................. 27 In`esDom, Ronel Bir´e, Vincent Hort, Gwena¨elleLavison-Bompard, Marina Nicolas and Thierry Gu´erin Extended Targeted and Non-Targeted Strategies for the Analysis of Marine Toxins in Mussels and Oysters by (LC-HRMS) Reprinted from: Toxins 2018, 10, 375, doi:10.3390/toxins10090375 .................. 42 Mirjam D. Klijnstra and Arjen Gerssen A Sensitive LC-MS/MS Method for Palytoxin Using Lithium Cationization Reprinted from: Toxins 2018, 10, 537, doi:10.3390/toxins10120537 .................. 64 Sarah C. Finch, Michael J. Boundy and D. Tim Harwood The Acute Toxicity of Tetrodotoxin and Tetrodotoxin–Saxitoxin Mixtures to Mice by Various Routes of Administration Reprinted from: Toxins 2018, 10, 423, doi:10.3390/toxins10110423 .................. 75 Arjen Gerssen, Toine H. F. Bovee, Mirjam D. Klijnstra, Marnix Poelman, Liza Portier and Ron L. A. P. Hoogenboom First Report on the Occurrence of Tetrodotoxins in Bivalve Mollusks in The Netherlands Reprinted from: Toxins 2018, 10, 450, doi:10.3390/toxins10110450 .................. 88 Benard Mucholwa Simiyu, Steve Omondi Oduor, Thomas Rohrlack, Lewis Sitoki and Rainer Kurmayer Microcystin Content in Phytoplankton and in Small Fish from Eutrophic Nyanza Gulf, Lake Victoria, Kenya Reprinted from: Toxins 2018, 10, 275, doi:10.3390/toxins10070275 ..................100 v Megan Brooke-Jones, Martina G´alikov´aand Heinrich Dircksen Cyanobacterial Neurotoxin Beta-Methyl-Amino-L-Alanine Affects Dopaminergic Neurons in Optic Ganglia and Brain of Daphnia magna Reprinted from: Toxins 2018, 10, 527, doi:10.3390/toxins10120527 ..................119 Valerio Zupo, Mirko Mutalipassi, Nadia Ruocco, Francesca Glaviano, Antonino Pollio, Antonio Luca Langellotti, Giovanna Romano and Maria Costantini Distribution of Toxigenic Halomicronema spp. in Adjacent Environments on the Island of Ischia: Comparison of Strains from Thermal Waters and Free Living in Posidonia Oceanica Meadows Reprinted from: Toxins 2019, 11, 99, doi:10.3390/toxins11020099 ...................136 Qiwen Liao, Guiyi Gong, Shirley Weng In Siu, Clarence Tsun Ting Wong, Huidong Yu, Yu Chung Tse, Gandhi R´adis-Baptistaand Simon Ming-Yuen Lee A Novel ShK-Like Toxic Peptide from the Transcriptome of the Cnidarian Palythoa caribaeorum Displays Neuroprotection and Cardioprotection in Zebrafish Reprinted from: Toxins 2018, 10, 238, doi:10.3390/toxins10060238 ..................154 David Wilson and Norelle L. Daly Nuclear Magnetic Resonance seq (NMRseq): A New Approach to Peptide Sequence Tags Reprinted from: Toxins 2018, 10, 437, doi:10.3390/toxins10110437 ..................170 Shiyong Zhang, Jia Li, Qin Qin, Wei Liu, Chao Bian, Yunhai Yi, Minghua Wang, Liqiang Zhong, Xinxin You, Shengkai Tang, Yanshan Liu, Yu Huang, Ruobo Gu, Junmin Xu, Wenji Bian, Qiong Shi and Xiaohui Chen Whole-Genome Sequencing of Chinese Yellow Catfish Provides a Valuable Genetic Resource for High-Throughput Identification of Toxin Genes Reprinted from: Toxins 2018, 10, 488, doi:10.3390/toxins10120488 ..................180 vi About the Special Issue Editors Ana Gago-Mart´ınez with a Ph.D Degree in Analytical Chemistry from the University of Vigo (Spain, 1992), Dr. Ana Gago-Mart´ınez leads a research team at the Department of Analytical and Food Chemistry at this same University. She graduated in Chemistry at the University of Santiago de Compostela (Spain, 1982), where she also obtained her Master’s Degree in Analytical Chemistry. In 1993, she continued her Post Doctoral studies for two years at the Institute of Marine Biosciences (National Research Council) in Halifax (Canada) and obtained a fellowship from the Galician and Spanish Ministry of Education as a guest scientist in Health Canada, Ottawa (Canada, 2000). Since 2009, Ana Gago Mart´ınez is the Director of the European Reference Laboratory for Marine Biotoxins. Arjen Gerssen with a Ph.D. Degree in Toxicology/Analytical Chemistry from the Wageningen University (The Netherlands, 2010), Dr Arjen Gerssen is senior scientist and food contaminants program manager at Wageningen Food Safety Research. He graduated in analytical chemistry at the university of applied sciences in Alkmaar, the Netherlands (2001). In 2004, he obtained his Master’s Degree in Analytical Chemistry at the Free University of Amsterdam. After obtaining his PhD degree in 2010, Arjen continued as a research scientist at Wageningen Food Safety Research and participated in various research projects on residues and contaminants in food. Since 2010, Arjen Gerssen is the scientist in charge of the national reference laboratory for Marine Biotoxins. vii toxins Editorial Emerging Marine Biotoxins Arjen Gerssen 1 and Ana Gago-Martínez 2,3,* 1 Wageningen Food Safety Research (WFSR), Wageningen University & Research, Akkermaalsbos 2, 6708WB Wageningen, The Netherlands; [email protected] 2 Department of Analytical and Food Chemistry, University of Vigo, Campus Universitario de Vigo, 36310 Vigo, Spain 3 European Union Reference Laboratory for Marine Biotoxins, CITEXVI, Campus Universitario de Vigo, 36310 Vigo, Spain * Correspondence: [email protected] Received: 28 May 2019; Accepted: 30 May 2019; Published: 3 June 2019 The emergence of marine biotoxins in geographical areas where they have never been reported before is a concern of considerable impact on seafood contamination, and consequently, on public health. Several groups of marine biotoxins, in particular tetrodotoxins, ciguatoxins, and palytoxins, are included among the relevant marine biotoxins that have recently emerged in several coastal areas. A similar situation has been observed in freshwater, where cyanobacterial toxins such as microcystins might end up in unexpected areas such as the estuaries where shellfish are cultivated. Climate change and the increased availability of nutrients have been considered as the key factors in the expansion of all of these toxins into new areas; however, this could also be due to more intense biological invasions, more sensitive analytical methods, or perhaps even an increased scientific interest in these natural contaminations. The incidences of human intoxications due to the consumption of seafood contaminated with these toxins have made their study an important task to accomplish, in order to protect human health. This special issue has a focus on a wide variety of emerging biotoxin classes. One of the most important classes of emerging toxins are ciguatoxins, which until recently were considered endemic to (sub)tropical regions in the Pacific and Indian Ocean as well as the Caribbean Sea, but are nowadays responsible for intoxications in other places worldwide. This is particularly so in Europe, not only through the consumption of imported ciguatoxin contaminated seafood from endemic areas, but also because of their occurrence in particular areas of Macaronesia such as Azores, Madeira Islands (Portugal) and the Canary
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