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Multiple New Paralytic Shellfish Toxin Vectors in Offshore

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Multiple New Paralytic Shellfish Toxin Vectors in Offshore marine drugs Article Multiple New Paralytic Shellfish Toxin Vectors in Offshore North Sea Benthos, a Deep Secret Exposed Karl J. Dean 1,*, Robert G. Hatfield 1, Vanessa Lee 1,2, Ryan P. Alexander 1, Adam M. Lewis 1, Benjamin H. Maskrey 1, Mickael Teixeira Alves 1 , Benjamin Hatton 3, Lewis N. Coates 1, Elisa Capuzzo 1, Jim R. Ellis 3 and Andrew D. Turner 1 1 Centre for Environment Fisheries and Aquaculture Science (Cefas), Barrack Road, Weymouth, Dorset DT4 8UB, UK; Robert.Hatfi[email protected] (R.G.H.); [email protected] (V.L.); [email protected] (R.P.A.); [email protected] (A.M.L.); [email protected] (B.H.M.); [email protected] (M.T.A.); [email protected] (L.N.C.); [email protected] (E.C.); [email protected] (A.D.T.) 2 Department of Chemistry, University of Surrey, Guildford, Surrey GU2 7XH, UK 3 Centre for Environment Fisheries and Aquaculture Science (Cefas), Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK; [email protected] (B.H.); [email protected] (J.R.E.) * Correspondence: [email protected] Received: 10 July 2020; Accepted: 25 July 2020; Published: 29 July 2020 Abstract: In early 2018, a large easterly storm hit the East Anglian coast of the UK, colloquially known as the ‘Beast from the East’, which also resulted in mass strandings of benthic organisms. There were subsequent instances of dogs consuming such organisms, leading to illness and, in some cases, fatalities. Epidemiological investigations identified paralytic shellfish toxins (PSTs) as the cause, with toxins present in a range of species and concentrations exceeding 14,000 µg STX eq./kg in the sunstar Crossaster papposus. This study sought to better elucidate the geographic spread of any toxicity and identify any key organisms of concern. During the summers of 2018 and 2019, various species of benthic invertebrates were collected from demersal trawl surveys conducted across a variety of locations in the North Sea. An analysis of the benthic epifauna using two independent PST testing methods identified a ‘hot spot’ of toxic organisms in the Southern Bight, with a mean toxicity of 449 µg STX eq./kg. PSTs were quantified in sea chervil (Alcyonidium diaphanum), the first known detection in the phylum bryozoan, as well as eleven other new vectors (>50 µg STX eq./kg), namely the opisthobranch Scaphander lignarius, the starfish Anseropoda placenta, Asterias rubens, Luidia ciliaris, Astropecten irregularis and Stichastrella rosea, the brittlestar Ophiura ophiura, the crustaceans Atelecyclus rotundatus and Munida rugosa, the sea mouse Aphrodita aculeata, and the sea urchin Psammechinus miliaris. The two species that showed consistently high PST concentrations were C. papposus and A. diaphanum. Two toxic profiles were identified, with one dominated by dcSTX (decarbamoylsaxitoxin) associated with the majority of samples across the whole sampling region. The second profile occurred only in North-Eastern England and consisted of mostly STX (Saxitoxin) and GTX2 (gonyautoxin 2). Consequently, this study highlights widespread and variable levels of PSTs in the marine benthos, together with the first evidence for toxicity in a large number of new species. These findings highlight impacts to ‘One Health’, with the unexpected sources of toxins potentially creating risks to animal, human and environmental health, with further work required to assess the severity and geographical/temporal extent of these impacts. Keywords: paralytic shellfish toxins; benthic organisms; starfish; saxitoxins; sunstar; sea chervil Mar. Drugs 2020, 18, 400; doi:10.3390/md18080400 www.mdpi.com/journal/marinedrugs Mar.Mar. Drugs Drugs2020 2020, 18, 18, 400, x FOR PEER REVIEW 2 of2 34 of 34 1. Introduction 1. Introduction Paralytic Shellfish Poisoning (PSP) is the human illness commonly associated with the Paralytic Shellfish Poisoning (PSP) is the human illness commonly associated with the consumption consumption of seafood that have bioaccumulated Paralytic Shellfish Toxins (PST) primarily in, but of seafood that have bioaccumulated Paralytic Shellfish Toxins (PST) primarily in, but not limited to, not limited to, bivalve molluscs [1,2]. A production of these toxins are associated with the formation bivalve molluscs [1,2]. A production of these toxins are associated with the formation of Harmful Algal of Harmful Algal Blooms (HABs), which are caused by certain specific phytoplankton species marine Blooms[3]. Specific (HABs), species which of are cyanobacteria caused by certain have specificalso been phytoplankton implicated in species the production marine [3]. of Specific PSTs speciesfrom offreshwater cyanobacteria environments have also [4]. been The implicated parent compound in the production saxitoxin of (STX), PSTs together from freshwater with many environments structurally- [4]. The parent compound saxitoxin (STX), together with many structurally-related analogues [5,6] (Figure1), related analogues [5,6] (Figure 1), are powerful neurotoxins that bind to site 1 of the Na+ voltage gated + arechannel powerful [5], neurotoxinsblocking synaptic that bind transmission. to site 1 of Sy themptoms Na voltage in humans gated include channel vomiting, [5], blocking headaches, synaptic transmission.dizziness, numbness Symptoms and in tingling humans of include extremities, vomiting, ataxia headaches, and paralysis, dizziness, and in numbnesssevere intoxications and tingling can of extremities,cause paralysis ataxia and and death paralysis, [7]. Consequently, and in severe intoxications to limit the risk can causeof human paralysis consumption and death of [7 contaminated]. Consequently, tobivalve limit the molluscs, risk of regulatory human consumption testing for the of contaminatedpresence of PSTs bivalve is a requirement molluscs, regulatory in a number testing of nations for the presence[8], with of a PSTsmaximum is a requirement permitted level in a number (MPL) of of 800 nations µg STX [8], witheq/ kg a of maximum flesh, defined permitted in legislation level (MPL) [9], of µ 800withg any STX bivalve eq/ kg of molluscs flesh, defined exhibiting in legislation total PST [ 9to],xicity with anyabove bivalve this threshold molluscs banned exhibiting from total commercial PST toxicity aboveharvest this and threshold human banned consumption. from commercial harvest and human consumption. Figure 1. Chemical structures of the commonly-reported Paralytic Shellfish Toxins (TEF = Toxicity Figure 1. Chemical structures of the commonly-reported Paralytic Shellfish Toxins (TEF = Toxicity EquivalenceEquivalence Factor Factor [10 [10]).]). ThereThere are are a a number number ofof cyanobacterialcyanobacterial genera know knownn to to produce produce saxitoxins saxitoxins [11–14] [11–14 of] of these these some some proliferateproliferate in in the the planktonic planktonic phasephase andand othersothers benthic.benthic. Benthic Benthic cyanobacterial cyanobacterial blooms blooms are are typically typically associatedassociated with with freshwater freshwater andand marginalmarginal marine habi habitiatstiats [11,15–17]. [11,15–17]. Benthic Benthic genera genera such such as asLyngbya Lyngbya havehave both both saxitoxin saxitoxin producing producing species species [11 [11,18],18] and and marine marine examples examples [15 [15],], however, however, marine marine species species are are not currentlynot currently known known to produce to produce saxitoxins saxitoxins and to and the authorsto the authors knowledge, knowledge, none of none the known of the PST known producing PST cyanobacteriaproducing cyanobacteria are present in are freshwater present in bodies freshwater in the UK.bodies Of thein the dinoflagellate UK. Of the PST dinoflagellate producers knownPST globally,producers the known genus Alexandriumglobally, the isgenus well Alexandrium represented inis well UK watersrepresented [19,20 in], withUK waters the other [19,20], PST producingwith the species,other PSTPyrodinium producing bahamense species,var. Pyrodiniumcompressum bahamenseand Gymnodinium var. compressum catenatum andbeing Gymnodinium absent. Of the catenatum species of being absent. Of the species of Alexandrium present in UK waters, three have been associated with PST production, A. minutum, A. catenella and A. ostenfeldii [21]. Within the UK, both A. catenella [19] and A. minutum [22] have been demonstrated to produce PST at high enough concentrations to cause human health issues in shellfish, whilst local populations of A. ostenfeldii have been found to produce only trace levels of PST [19]. The genus Alexandrium is also a well-documented producer of resilient cysts [21]. Cyst deposits can be dense [23], and span wide geographic areas [23–25]. Grazing on cysts Mar. Drugs 2020, 18, 400 3 of 34 Alexandrium present in UK waters, three have been associated with PST production, A. minutum, A. catenella and A. ostenfeldii [21]. Within the UK, both A. catenella [19] and A. minutum [22] have been demonstrated to produce PST at high enough concentrations to cause human health issues in shellfish, whilst local populations of A. ostenfeldii have been found to produce only trace levels of PST [19]. The genus Alexandrium is also a well-documented producer of resilient cysts [21]. Cyst deposits can be dense [23], and span wide geographic areas [23–25]. Grazing on cysts has been shown to be a route of toxin accumulation in shellfish [26]. This suggests that benthic organisms, especially those feeding in sediment or filter feeding from the water directly over the sediment, could be exposed to
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