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EARLY ONLINE RELEASE Posted October 26, 2018 OceTHE OFFICIALa MAGAZINEn ogOF THE OCEANOGRAPHYra SOCIETYphy EARLY ONLINE RELEASE Posted October 26, 2018 CITATION Krock, B., M.E. Ferrario, R. Akselman, and N.G. Montoya. 2018. Occurrence of marine bio- toxins and shellfish poisoning events and their causative organisms in Argentine marine waters. Oceanography 31(4), https://doi.org/10.5670/oceanog.2018.403. DOI https://doi.org/10.5670/oceanog.2018.403 PERMISSIONS Oceanography (ISSN 1042-8275) is published by The Oceanography Society, 1 Research Court, Suite 450, Rockville, MD 20850 USA. ©2018 The Oceanography Society, Inc. Permission is granted for individuals to read, download, copy, distribute, print, search, and link to the full texts of Oceanography articles. 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DOWNLOADED FROM HTTPS://TOS.ORG/OCEANOGRAPHY SPECIAL ISSUE ON THE GULF OF SAN JORGE Occurrence of MARINE BIOTOXINS AND SHELLFISH POISONING EVENTS and Their Causative Organisms in Argentine Marine Waters By Bernd Krock, Martha E. Ferrario, Rut Akselman, and Nora G. Montoya Micrographs courtesy of Urban Tillmann, AWI; Background NOAA photo courtesy of Vera Trainer Oceanography48 Oceanography | Vol.31, | NoVol.4.31, | NoEarly.4 Online Release ABSTRACT. In the Argentine Sea, marine phycotoxins of microalgal origin associated Santinelli et al., 1994a, 2002; Cadaillón, with five shellfish poisoning syndromes have been reported. The most problematic in 2012; Sunesen et al., 2014; Krock et al., terms of toxicity and geographic distribution is paralytic shellfish poisoning (PSP), fol- 2015a), lowed by diarrhetic shellfish poisoning (DSP). In contrast, amnesic shellfish poisoning 3. Spiroimine shellfish poisoning (SSP) (ASP), spiroimine shellfish poisoning (SSP), and azaspiracid shellfish poisoning (AZP) (Almandoz et al., 2014; Fabro et al., have not been reported to cause human illness or closures of shellfish harvest sites in 2017), Argentina to date but pose a potential risk, as associated toxins and producing organ- 4. Diarrhetic shellfish poisoning (DSP; isms are present in Southwest Atlantic waters and were detected at subregulatory lev- Gayoso et al., 2002; Sar et al., 2010, els in mollusks. Alexandrium catenella and Gymnodinium catenatum have been iden- 2012; Montoya et al., 2011; Sunesen tified as producers of the PSP toxins C1/2, gonyautoxins (GTX1-4), saxitoxin (STX), et al., 2014; Gracia Villalobos et al., and neosaxitoxin (NEO) in the Argentine Sea. Nine potentially toxigenic species of 2015; Krock et al., 2015a; Turner and the diatom genus Pseudo-nitzschia have been reported for Argentinean coastal waters: Goya, 2015; Akselman et al., 2015; P. australis, P. brasiliana, P. delicatissima, P. fraudulenta, P. multiseries, P. pseudodelica- Fabro et al., 2015, 2016), and tissima, P. pungens, P. seriata, and P. turgidula, all of which are known to produce the 5. Azaspiracid shellfish poisoning (AZP; neurotoxin domoic acid that causes ASP. Two genera have been identified as produc- Turner and Goya, 2015; Tillmann ers of DSP toxins in Argentina: the benthic dinoflagellate Prorocentrum lima and sev- et al., 2016). eral species of the pelagic dinoflagellate genus Dinophysis: D. acuminata, D. caudata, D. fortii, D. norvegica, and D. tripos. The occurrence of these species in Argentine waters This review compiles the recent is associated with okadaic acid (OA), dinophysistoxin-1 (DTX-1), pectenotoxin-2 knowledge on the occurrence of toxi- (PTX-2), and pectenotoxin-2 seco acid (PTX-2sa). Historically, yessotoxins (YTXs) genic microalgae and their phycotoxins were also included in DSP syndrome and all three known YTX-producers have been in this region. confirmed in Argentinean waters: Gonyaulax spinifera, Lingulodinium polyedra, and Protoceratium reticulatum, but of these only P. reticulatum could be associated with YTX PARALYTIC SHELLFISH production to date. Several species of the family Amphidomataceae, which cause AZP, POISONING (PSP) have been reported for Argentina: Amphidoma languida, Azadinium dexteroporum, PSP toxins are among the most toxic Az. luciferelloides, Az. poporum, and Az. spinosum. In Argentinean coastal waters, out marine biotoxins. In addition to causing of these species only Az. poporum has been identified as toxigenic to date, as it produces muscular paralysis, they have been respon- azaspiracid-2 (AZA-2) and its phosphorylated form. Currently in Argentina, seafood is sible for hundreds of human fatalities monitored for the risk of ASP, AZP, DSP, and PSP. (Hallegraeff, 1995). Comprising a group of hydrated purine derivatives, variations INTRODUCTION organisms, among which shellfish are the consist of hydroxylation at N1, sulpha- Toxic marine microalgae are usually most relevant for humans. tation at C11, and various substitutions at responsible for human shellfish poisoning Shellfish poisoning events are catego- C13, which can be hydroxylation (decar- events. They produce secondary metabo- rized according to the symptoms they bamoyl toxins), carbamoylation (car- lites that may be taken up and concen- induce in humans. Although not all bamoyl toxins), N-sulfocarbamoylation trated to high levels by filter-feeding mol- types of shellfish poisoning syndromes (N-sulfocarbamoyl toxins), benzoylation lusks and cause severe illnesses or even have been reported to date in Argentine (benzoyl toxins), and all combinations death in vertebrates (including humans) waters, several toxigenic microalgal spe- of these substitutions (Figure 1a). Due to after consumption of contaminated shell- cies and their toxins have been identi- two guanidine moieties in the molecule, fish. Interestingly, these marine bio- fied in this region during the last four PSP toxins are charged and thus highly toxins usually trigger no or few adverse decades. They cause five different shell- hydrophilic in contrast to most other effects in primary consumers of toxic fish poisoning syndromes: phycotoxins. The positive charges and microalgae, such as crustaceans and mol- 1. Amnesic shellfish poisoning (ASP; the structural configuration of PSP tox- lusks. The low toxic effect of marine bio- Montoya et al., 2000, 2008; R.M. ins enable them to efficiently bind to and toxins on their direct predators seems to Negri et al., 2004; Sastre et al., 2007; block voltage-dependent ion channels argue against the function of marine bio- Cadaillón, 2012; Krock et al., 2015a; in neuronal cells, which inhibits sodium toxins as a defense mechanism against Almandoz et al., 2017), influx into excited cells and thus inhibits predation. In fact, the ecological function 2. Paralytic shellfish poisoning (PSP; signal relaxation (Hall et al., 1987). of marine biotoxins is still unknown. We Carreto et al., 1981, 1986, 1998, 2007; The intraperitoneal toxicity of saxi- do know that the phycotoxins produced Esteves et al., 1992; Benavides et al., toxin (the most potent of the PSP toxins) –1 by microalgae are easily accumulated and 1995; Akselman et al., 1998; Gayoso, in mice (LD50) is 8 µg kg body weight concentrated by filter-feeding marine 2001; Montoya et al., 2006, 2018; (Baden et al., 1995). However, toxicity of Oceanography | December 2018 | https://doi.org/10.5670/oceanog.2018.403 individual variants can differ over more For this reason, monitoring of biotoxins recommended by the European Union than two orders of magnitude, depend- in mollusks is important in the regulation Toxicology Working Group (WG; FAO, ing on the net charge of the toxins and of seafood (Etheridge, 2010). 2006). To comply with European regula- their structural configuration. In con- Unpredictable toxic blooms often tions and to ensure consumer protection, trast to many other marine biotoxins, affect both commercial harvest areas monitoring of toxic phytoplankton in the which show a lower oral than intraperi- and aquaculture facilities. In addition water and PSP toxins in shellfish is a stat- toneal toxicity, both routes of applica- to seafood regulation and monitoring utory requirement for EU member states tion are efficient for PSP toxins, and thus of shellfish for biotoxins, in many cases and for others desiring to export shell- PSP toxinsA are considered a high risk for phytoplanktonB monitoring has been fish products to countries within the EU shellfish consumers (Hallegraeff, 1995). established as a preventive measure, as (Anonymous, 2004a). O 31 Sanitary standards for the export of O 35 34 2 live bivalve mollusks from Argentina are 3 N based on Regulation (EC) No. 853/2004 regarding the regulated toxins and their OH A B O respective legislated limits. The con- b O trol system and monitoring of toxins in 13 O O 31 A B O HO A 35 34 B Argentina was initiated in 1980, after 2 a 3 N lethal poisonings of two fishermen caused O 31 O 35 34 O 31 O 35 34 by consumption of PSP-contaminated
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