Co-occurrence of Marine and Freshwater Phycotoxins in Oysters, and Analysis of Possible Predictors for Management

Overview

Journal Toxicon X

Specialty Toxicology

Date 2023 Jul 14

PMID 37448555

Authors

Sarah K D Pease

Todd A Egerton

Kimberly S Reece

Marta P Sanderson

Michelle D Onofrio

Evan Yeargan

Adam Wood

Amanda Roach

I-Shuo Wade Huang

Gail P Scott

Allen R Place

Amy M Hayes

Juliette L Smith

Affiliations

Soon will be listed here.

Abstract

Oysters () were screened for 12 phycotoxins over two years in nearshore waters to collect baseline phycotoxin data and to determine prevalence of phycotoxin co-occurrence in the commercially and ecologically-relevant species. Trace to low concentrations of azaspiracid-1 and -2 (AZA1, AZA2), domoic acid (DA), okadaic acid (OA), and dinophysistoxin-1 (DTX1) were detected, orders of magnitude below seafood safety action levels. Microcystins (MCs), MC-RR and MC-YR, were also found in oysters (maximum: 7.12 μg MC-RR/kg shellfish meat wet weight), warranting consideration of developing action levels for freshwater phycotoxins in marine shellfish. Oysters contained phycotoxins that impair shellfish health: karlotoxin1-1 and 1-3 (KmTx1-1, KmTx1-3), goniodomin A (GDA), and pectenotoxin-2 (PTX2). Co-occurrence of phycotoxins in oysters was common (54%, n = 81). AZAs and DA co-occurred most frequently of the phycotoxins investigated that are a concern for human health (n = 13) and PTX2 and KmTxs co-occurred most frequently amongst the phycotoxins of concern for shellfish health (n = 9). Various harmful algal bloom (HAB) monitoring methods and tools were assessed for their effectiveness at indicating levels of phycotoxins in oysters. These included co-deployed solid phase adsorption toxin tracking (SPATT) devices, toxin levels in particulate organic matter (POM, >1.5 μm) and whole water samples and cell concentrations from water samples as determined by microscopy and quantitative real-time PCR (qPCR). The dominant phycotoxin varied between SPATTs and all other phycotoxin sample types, and out of the 11 phycotoxins detected in oysters, only four and seven were detected in POM and whole water respectively, indicating phycotoxin profile mismatch between ecosystem compartments. Nevertheless, there were correlations between DA in oysters and whole water (simple linear regression [LR]: R = 0.6, p < 0.0001, n = 40), and PTX2 in oysters and SPATTs (LR: R = 0.3, p = 0.001, n = 36), providing additional monitoring tools for these phycotoxins, but oyster samples remain the best overall indicators of seafood safety.

References

Onofrio M, Mallet C, Place A, Smith J . A Screening Tool for the Direct Analysis of Marine and Freshwater Phycotoxins in Organic SPATT Extracts from the Chesapeake Bay. Toxins (Basel). 2020; 12(5). PMC: 7290987. DOI: 10.3390/toxins12050322. View

Wang X, Chen Y, Zuo X, Ding N, Zeng H, Zou X . Microcystin (-LR) induced testicular cell apoptosis via up-regulating apoptosis-related genes in vivo. Food Chem Toxicol. 2013; 60:309-17. DOI: 10.1016/j.fct.2013.07.039. View

Harris C, Reece K, Stec D, Scott G, Jones W, Hobbs P . The toxin goniodomin, produced by Alexandrium spp., is identical to goniodomin A. Harmful Algae. 2020; 92:101707. DOI: 10.1016/j.hal.2019.101707. View

Camacho-Munoz D, Waack J, Turner A, Lewis A, Lawton L, Edwards C . Rapid uptake and slow depuration: Health risks following cyanotoxin accumulation in mussels?. Environ Pollut. 2021; 271:116400. PMC: 7859834. DOI: 10.1016/j.envpol.2020.116400. View

Straquadine N, Kudela R, Gobler C . Hepatotoxic shellfish poisoning: Accumulation of microcystins in Eastern oysters (Crassostrea virginica) and Asian clams (Corbicula fluminea) exposed to wild and cultured populations of the harmful cyanobacteria, Microcystis. Harmful Algae. 2022; 115:102236. DOI: 10.1016/j.hal.2022.102236. View

Vareli K, Jaeger W, Touka A, Frillingos S, Briasoulis E, Sainis I . Hepatotoxic seafood poisoning (HSP) due to microcystins: a threat from the ocean?. Mar Drugs. 2013; 11(8):2751-68. PMC: 3766863. DOI: 10.3390/md11082751. View

Eriksson J, Toivola D, Meriluoto J, Karaki H, Han Y, HARTSHORNE D . Hepatocyte deformation induced by cyanobacterial toxins reflects inhibition of protein phosphatases. Biochem Biophys Res Commun. 1990; 173(3):1347-53. DOI: 10.1016/s0006-291x(05)80936-2. View

Bouaicha N, Miles C, Beach D, Labidi Z, Djabri A, Benayache N . Structural Diversity, Characterization and Toxicology of Microcystins. Toxins (Basel). 2019; 11(12). PMC: 6950048. DOI: 10.3390/toxins11120714. View

Li Y, Sheng J, Sha J, Han X . The toxic effects of microcystin-LR on the reproductive system of male rats in vivo and in vitro. Reprod Toxicol. 2008; 26(3-4):239-45. DOI: 10.1016/j.reprotox.2008.09.004. View

10.

Trainer V, Moore L, Bill B, Adams N, Harrington N, Borchert J . Diarrhetic shellfish toxins and other lipophilic toxins of human health concern in Washington State. Mar Drugs. 2013; 11(6):1815-35. PMC: 3721207. DOI: 10.3390/md11061815. View

11.

Huang I, Zimba P . Cyanobacterial bioactive metabolites-A review of their chemistry and biology. Harmful Algae. 2019; 83:42-94. DOI: 10.1016/j.hal.2018.11.008. View

12.

Roue M, Darius H, Chinain M . Solid Phase Adsorption Toxin Tracking (SPATT) Technology for the Monitoring of Aquatic Toxins: A Review. Toxins (Basel). 2018; 10(4). PMC: 5923333. DOI: 10.3390/toxins10040167. View

13.

Luo Z, Krock B, Neil Mertens K, Price A, Turner R, Rabalais N . Morphology, molecular phylogeny and azaspiracid profile of Azadinium poporum (Dinophyceae) from the Gulf of Mexico. Harmful Algae. 2017; 55:56-65. DOI: 10.1016/j.hal.2016.02.006. View

14.

Place A, Munday R, Munday J . Acute toxicity of karlotoxins to mice. Toxicon. 2014; 90:184-90. PMC: 4498405. DOI: 10.1016/j.toxicon.2014.08.003. View

15.

Pestana C, Reeve P, Newcombe G . Extraction method for total microcystins in cyanobacteria-laden sludge. J Chromatogr B Analyt Technol Biomed Life Sci. 2014; 965:61-4. DOI: 10.1016/j.jchromb.2014.06.012. View

16.

Miller M, Kudela R, Mekebri A, Crane D, Oates S, Tinker M . Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters. PLoS One. 2010; 5(9). PMC: 2936937. DOI: 10.1371/journal.pone.0012576. View

17.

Pease S, Reece K, OBrien J, Hobbs P, Smith J . Oyster hatchery breakthrough of two HABs and potential effects on larval eastern oysters (Crassostrea virginica). Harmful Algae. 2021; 101:101965. DOI: 10.1016/j.hal.2020.101965. View

18.

Mulvenna V, Dale K, Priestly B, Mueller U, Humpage A, Shaw G . Health risk assessment for cyanobacterial toxins in seafood. Int J Environ Res Public Health. 2012; 9(3):807-20. PMC: 3367279. DOI: 10.3390/ijerph9030807. View

19.

Ohta T, Nishiwaki S, Suganuma M, Kohyama K, Ishikawa T, Carmichael W . Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. J Cancer Res Clin Oncol. 1992; 118(6):420-4. DOI: 10.1007/BF01629424. View

20.

Garca C, Mardones P, Sfeir A, Lagos N . Simultaneous presence of paralytic and diarrheic shellfish poisoning toxins in Mytilus chilensis samples collected in the Chiloe Island, Austral Chilean fjords. Biol Res. 2004; 37(4 Suppl A):721-31. DOI: 10.4067/s0716-97602004000500002. View