Dihydrodinophysistoxin-1 Produced by Dinophysis norvegica in the Gulf of Maine, USA and Its Accumulation in Shellfish

Deeds, Jonathan R.; Stutts, Whitney L.; Celiz, Mary Dawn; MacLeod, Jill; Hamilton, Amy E.; Lewis, Bryant J.; Miller, David W.; Kanwit, Kohl; Smith, Juliette L.; Kulis, David M.; McCarron, Pearse; Rauschenberg, Carlton D.; Burnell, Craig A.; Archer, Stephen D.; Borchert, Jerry; Lankford, Shelley K.

doi:10.3390/toxins12090533

Open AccessArticle

Dihydrodinophysistoxin-1 Produced by Dinophysis norvegica in the Gulf of Maine, USA and Its Accumulation in Shellfish

by

Jonathan R. Deeds

^1,*,

Whitney L. Stutts

^1,†,

Mary Dawn Celiz

¹,

Jill MacLeod

²,

Amy E. Hamilton

^2,‡,

Bryant J. Lewis

²,

David W. Miller

²,

Kohl Kanwit

²,

Juliette L. Smith

³,

David M. Kulis

⁴,

Pearse McCarron

⁵,

Carlton D. Rauschenberg

⁶,

Craig A. Burnell

⁶,

Stephen D. Archer

⁶,

Jerry Borchert

⁷ and

Shelley K. Lankford

⁸

¹

Office of Regulatory Science, United States Food and Drug Administration, Center for Food Safety and Applied Nutrition, College Park, MD 20740, USA

²

Maine Department of Marine Resources, West Boothbay Harbor, ME 05475, USA

³

Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA 23062, USA

⁴

Department of Biology, Woods Hole Oceanographic Institute, Woods Hole, MA 02543, USA

⁵

Biotoxin Metrology, National Research Council Canada, Halifax, NS B3H 3Z1, Canada

⁶

Bigelow Analytical Services, Bigelow Laboratory for Ocean Sciences, East Boothbay, ME 04544, USA

⁷

Washington State Department of Health, Olympia, WA 98504, USA

⁸

Washington State Department of Health Public Health Laboratories, Shoreline, WA 98155, USA

^*

Author to whom correspondence should be addressed.

^†

Current Address: Molecular Education, Technology, and Research Innovation Center, North Carolina State University, Raleigh, NC 27695, USA.

^‡

Current Address: Tidewater Ecosystem Assessment, Maryland Department of Natural Resources, Annapolis, MD 21401, USA.

Toxins 2020, 12(9), 533; https://doi.org/10.3390/toxins12090533

Submission received: 25 July 2020 / Revised: 12 August 2020 / Accepted: 17 August 2020 / Published: 20 August 2020

(This article belongs to the Special Issue Marine Toxins from Harmful Algae and Seafood Safety)

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Abstract

Dihydrodinophysistoxin-1 (dihydro-DTX1, (M-H)⁻m/z 819.5), described previously from a marine sponge but never identified as to its biological source or described in shellfish, was detected in multiple species of commercial shellfish collected from the central coast of the Gulf of Maine, USA in 2016 and in 2018 during blooms of the dinoflagellate Dinophysis norvegica. Toxin screening by protein phosphatase inhibition (PPIA) first detected the presence of diarrhetic shellfish poisoning-like bioactivity; however, confirmatory analysis using liquid chromatography-tandem mass spectrometry (LC-MS/MS) failed to detect okadaic acid (OA, (M-H)⁻m/z 803.5), dinophysistoxin-1 (DTX1, (M-H)⁻m/z 817.5), or dinophysistoxin-2 (DTX2, (M-H)⁻m/z 803.5) in samples collected during the bloom. Bioactivity-guided fractionation followed by liquid chromatography-high resolution mass spectrometry (LC-HRMS) tentatively identified dihydro-DTX1 in the PPIA active fraction. LC-MS/MS measurements showed an absence of OA, DTX1, and DTX2, but confirmed the presence of dihydro-DTX1 in shellfish during blooms of D. norvegica in both years, with results correlating well with PPIA testing. Two laboratory cultures of D. norvegica isolated from the 2018 bloom were found to produce dihydro-DTX1 as the sole DSP toxin, confirming the source of this compound in shellfish. Estimated concentrations of dihydro-DTX1 were >0.16 ppm in multiple shellfish species (max. 1.1 ppm) during the blooms in 2016 and 2018. Assuming an equivalent potency and molar response to DTX1, the authority initiated precautionary shellfish harvesting closures in both years. To date, no illnesses have been associated with the presence of dihydro-DTX1 in shellfish in the Gulf of Maine region and studies are underway to determine the potency of this new toxin relative to the currently regulated DSP toxins in order to develop appropriate management guidance.

Keywords: diarrhetic shellfish poisoning; dihydro-DTX1; Dinophysis norvegica; Gulf of Maine USA

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MDPI and ACS Style

Deeds, J.R.; Stutts, W.L.; Celiz, M.D.; MacLeod, J.; Hamilton, A.E.; Lewis, B.J.; Miller, D.W.; Kanwit, K.; Smith, J.L.; Kulis, D.M.; et al. Dihydrodinophysistoxin-1 Produced by Dinophysis norvegica in the Gulf of Maine, USA and Its Accumulation in Shellfish. Toxins 2020, 12, 533. https://doi.org/10.3390/toxins12090533

AMA Style

Deeds JR, Stutts WL, Celiz MD, MacLeod J, Hamilton AE, Lewis BJ, Miller DW, Kanwit K, Smith JL, Kulis DM, et al. Dihydrodinophysistoxin-1 Produced by Dinophysis norvegica in the Gulf of Maine, USA and Its Accumulation in Shellfish. Toxins. 2020; 12(9):533. https://doi.org/10.3390/toxins12090533

Chicago/Turabian Style

Deeds, Jonathan R., Whitney L. Stutts, Mary Dawn Celiz, Jill MacLeod, Amy E. Hamilton, Bryant J. Lewis, David W. Miller, Kohl Kanwit, Juliette L. Smith, David M. Kulis, and et al. 2020. "Dihydrodinophysistoxin-1 Produced by Dinophysis norvegica in the Gulf of Maine, USA and Its Accumulation in Shellfish" Toxins 12, no. 9: 533. https://doi.org/10.3390/toxins12090533

APA Style

Deeds, J. R., Stutts, W. L., Celiz, M. D., MacLeod, J., Hamilton, A. E., Lewis, B. J., Miller, D. W., Kanwit, K., Smith, J. L., Kulis, D. M., McCarron, P., Rauschenberg, C. D., Burnell, C. A., Archer, S. D., Borchert, J., & Lankford, S. K. (2020). Dihydrodinophysistoxin-1 Produced by Dinophysis norvegica in the Gulf of Maine, USA and Its Accumulation in Shellfish. Toxins, 12(9), 533. https://doi.org/10.3390/toxins12090533

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Dihydrodinophysistoxin-1 Produced by Dinophysis norvegica in the Gulf of Maine, USA and Its Accumulation in Shellfish

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