Publications by authors named "Juliette L Smith"

19 Publications

  • Page 1 of 1

Spatiotemporal distribution of phycotoxins and their co-occurrence within nearshore waters.

Harmful Algae 2021 03 10;103:101993. Epub 2021 Feb 10.

Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA 23062, USA. Electronic address:

Harmful algal blooms (HABs), varying in intensity and causative species, have historically occurred throughout the Chesapeake Bay, U.S.; however, phycotoxin data are sparse. The spatiotemporal distribution of phycotoxins was investigated using solid-phase adsorption toxin tracking (SPATT) across 12 shallow, nearshore sites within the lower Chesapeake Bay and Virginia's coastal bays over one year (2017-2018). Eight toxins, azaspiracid-1 (AZA1), azaspiracid-2 (AZA2), microcystin-LR (MC-LR), domoic acid (DA), okadaic acid (OA), dinophysistoxin-1 (DTX1), pectenotoxin-2 (PTX2), and goniodomin A (GDA) were detected in SPATT extracts. Temporally, phycotoxins were always present in the region, with at least one phycotoxin group (i.e., consisting of OA and DTX1) detected at every time point. Co-occurrence of phycotoxins was also common; two or more toxin groups were observed in 76% of the samples analyzed. Toxin maximums: 0.03 ng AZA2/g resin/day, 0.25 ng DA/g resin/day, 15 ng DTX1/g resin/day, 61 ng OA/g resin/day, 72 ng PTX2/g resin/day, and 102,050 ng GDA/g resin/day were seasonal, with peaks occurring in summer and fall. Spatially, the southern tributary and coastal bay regions harbored the highest amount of total phycotoxins on SPATT over the year, and the former contained the greatest diversity of phycotoxins. The novel detection of AZAs in the region, before a causative species has been identified, supports the use of SPATT as an explorative tool in respect to emerging threats. The lack of karlotoxin in SPATT extracts, but detection of Karlodinium veneficum by microscopy, however, emphasizes that this tool should be considered complementary to, but not a replacement for, more traditional HAB management and monitoring methods.
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http://dx.doi.org/10.1016/j.hal.2021.101993DOI Listing
March 2021

Marine harmful algal blooms (HABs) in the United States: History, current status and future trends.

Harmful Algae 2021 02 3;102:101975. Epub 2021 Mar 3.

Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, WA, 98112, United States.

Harmful algal blooms (HABs) are diverse phenomena involving multiple. species and classes of algae that occupy a broad range of habitats from lakes to oceans and produce a multiplicity of toxins or bioactive compounds that impact many different resources. Here, a review of the status of this complex array of marine HAB problems in the U.S. is presented, providing historical information and trends as well as future perspectives. The study relies on thirty years (1990-2019) of data in HAEDAT - the IOC-ICES-PICES Harmful Algal Event database, but also includes many other reports. At a qualitative level, the U.S. national HAB problem is far more extensive than was the case decades ago, with more toxic species and toxins to monitor, as well as a larger range of impacted resources and areas affected. Quantitatively, no significant trend is seen for paralytic shellfish toxin (PST) events over the study interval, though there is clear evidence of the expansion of the problem into new regions and the emergence of a species that produces PSTs in Florida - Pyrodinium bahamense. Amnesic shellfish toxin (AST) events have significantly increased in the U.S., with an overall pattern of frequent outbreaks on the West Coast, emerging, recurring outbreaks on the East Coast, and sporadic incidents in the Gulf of Mexico. Despite the long historical record of neurotoxic shellfish toxin (NST) events, no significant trend is observed over the past 30 years. The recent emergence of diarrhetic shellfish toxins (DSTs) in the U.S. began along the Gulf Coast in 2008 and expanded to the West and East Coasts, though no significant trend through time is seen since then. Ciguatoxin (CTX) events caused by Gambierdiscus dinoflagellates have long impacted tropical and subtropical locations in the U.S., but due to a lack of monitoring programs as well as under-reporting of illnesses, data on these events are not available for time series analysis. Geographic expansion of Gambierdiscus into temperate and non-endemic areas (e.g., northern Gulf of Mexico) is apparent, and fostered by ocean warming. HAB-related marine wildlife morbidity and mortality events appear to be increasing, with statistically significant increasing trends observed in marine mammal poisonings caused by ASTs along the coast of California and NSTs in Florida. Since their first occurrence in 1985 in New York, brown tides resulting from high-density blooms of Aureococcus have spread south to Delaware, Maryland, and Virginia, while those caused by Aureoumbra have spread from the Gulf Coast to the east coast of Florida. Blooms of Margalefidinium polykrikoides occurred in four locations in the U.S. from 1921-2001 but have appeared in more than 15  U.S. estuaries since then, with ocean warming implicated as a causative factor. Numerous blooms of toxic cyanobacteria have been documented in all 50  U.S. states and the transport of cyanotoxins from freshwater systems into marine coastal waters is a recently identified and potentially significant threat to public and ecosystem health. Taken together, there is a significant increasing trend in all HAB events in HAEDAT over the 30-year study interval. Part of this observed HAB expansion simply reflects a better realization of the true or historic scale of the problem, long obscured by inadequate monitoring. Other contributing factors include the dispersion of species to new areas, the discovery of new HAB poisoning syndromes or impacts, and the stimulatory effects of human activities like nutrient pollution, aquaculture expansion, and ocean warming, among others. One result of this multifaceted expansion is that many regions of the U.S. now face a daunting diversity of species and toxins, representing a significant and growing challenge to resource managers and public health officials in terms of toxins, regions, and time intervals to monitor, and necessitating new approaches to monitoring and management. Mobilization of funding and resources for research, monitoring and management of HABs requires accurate information on the scale and nature of the national problem. HAEDAT and other databases can be of great value in this regard but efforts are needed to expand and sustain the collection of data regionally and nationally.
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http://dx.doi.org/10.1016/j.hal.2021.101975DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8058451PMC
February 2021

Oyster hatchery breakthrough of two HABs and potential effects on larval eastern oysters (Crassostrea virginica).

Harmful Algae 2021 01 26;101:101965. Epub 2020 Dec 26.

Virginia Institute of Marine Science, William & Mary, P.O. Box 1346, Gloucester Point, VA 23062, USA. Electronic address:

Harmful algal bloom (HAB) dinoflagellate species Karlodinium veneficum and Prorocentrum cordatum (prev. P. minimum) are commonly found in Chesapeake Bay during the late spring and early summer months, coinciding with the spawning season of the eastern oyster (Crassostrea virginica). Unexplained larval oyster mortalities at regional commercial hatcheries prompted screening of oyster hatchery water samples for these HAB species. Both HAB species were found in treated hatchery water during the oyster spawning season, sometimes exceeding bloom cell concentrations (≥ 1,000 cells/mL). To investigate the potential for these HAB species, independently or in co-exposure, to affect larval oyster mortality and activity, 96-h laboratory single and dual HAB bioassays with seven-day-old oyster larvae were performed. Treatments for the single HAB bioassay included fed and unfed controls, K. veneficum at 1,000; 5,000; 10,000; and 50,000 cells/mL, P. cordatum at 100; 5,000; 10,000; and 50,000 cells/mL. Subsequently, the 1,000 cells/mL K. veneficum and 50,000 cells/mL P. cordatum treatments were combined in a co-exposure treatment for the dual HAB bioassay. At all cell concentrations tested, K. veneficum swarmed oyster larvae and caused significant larval oyster mortality by 96 h (Karlo: 21 ± 5%; Karlo: 93 ± 2%; Karlo: 85 ± 3%; Karlo: 83 ± 5%, SE). In contrast, there was no significant difference in larval oyster mortality between the control treatments and any of the P. cordatum treatments by 96 h. By 24 h, larval oysters were significantly less active (immotile) in the presence of either HAB species as compared to control treatments (e.g., Karlo: 37.8 ± 4.1%; Proro: 47.3 ± 7.4%; Fed: 10.8 ± 3.2%; Unfed: 10.1 ± 4.9%, SE). In the dual HAB bioassay, larval oyster mortality associated with 1,000 cells/mL K. veneficum (44 ± 9%, SE) was not changed by the addition of 50,000 cells/mL P. cordatum (55 ± 7%, SE), demonstrating that K. veneficum was primarily responsible for the observed mortality. This study demonstrated that even low cell concentrations of K. veneficum and P. cordatum are harmful to larval oysters, and could contribute to reductions in oyster hatchery production through impacts on this critical life stage.
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http://dx.doi.org/10.1016/j.hal.2020.101965DOI Listing
January 2021

Growth response of Dinophysis, Mesodinium, and Teleaulax cultures to temperature, irradiance, and salinity.

Harmful Algae 2020 09 29;98:101896. Epub 2020 Aug 29.

Department of Oceanography, Texas A&M University, College Station, TX 77843, USA. Electronic address:

Mixotrophic Dinophysis species threaten human health and coastal economies through the production of toxins which cause diarrhetic shellfish poisoning (DSP) in humans. Novel blooms of Dinophysis acuminata and Dinophysis ovum have occurred in North American waters in recent decades, resulting in the closure of shellfish harvesting. Understanding the ecology of Dinophysis species and their prey is essential to predicting and mitigating the impact of blooms of these dinoflagellates. The growth response of two new isolates of Dinophysis species, one isolate of Mesodinium rubrum, and two strains of Teleaulax amphioxeia were evaluated at a range of temperature, salinity, and irradiance treatments to identify possible environmental drivers of Dinophysis blooms in the Gulf of Mexico. Results showed optimal growth of T. amphioxeia and M. rubrum at 24 °C, salinity 30 - 34, and irradiances between 300 and 400 µmol quanta m  s  . Optimal Dinophysis growth was observed at salinity 22 and temperatures between 18 and 24 °C. Mesodinium and both Dinophysis responded differently to experimental treatments, which may be due to the suitability of prey and different handling of kleptochloroplasts. Dinophysis bloom onset may be initiated by warming surface waters between winter and spring in the Gulf of Mexico. Toxin profiles for these two North American isolates were distinct; Dinophysis acuminata produced okadaic acid, dinophysistoxin-1, and pectenotoxin-2 while D. ovum produced only okadaic acid. Toxin per cell for D. ovum was two orders of magnitude greater than D. acuminata. Phylogenies based on the cox1 and cob genes did not distinguish these two Dinophysis species within the D. acuminata complex.
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http://dx.doi.org/10.1016/j.hal.2020.101896DOI Listing
September 2020

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

Toxins (Basel) 2020 08 20;12(9). Epub 2020 Aug 20.

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

Dihydrodinophysistoxin-1 (dihydro-DTX1, (M-H) 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 . 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) 803.5), dinophysistoxin-1 (DTX1, (M-H) 817.5), or dinophysistoxin-2 (DTX2, (M-H) 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 in both years, with results correlating well with PPIA testing. Two laboratory cultures of 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.
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http://dx.doi.org/10.3390/toxins12090533DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7551465PMC
August 2020

A Screening Tool for the Direct Analysis of Marine and Freshwater Phycotoxins in Organic SPATT Extracts from the Chesapeake Bay.

Toxins (Basel) 2020 05 13;12(5). Epub 2020 May 13.

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

Many detection methods for phycotoxins, bioactive compounds produced by harmful algae, focus on one compound or a class of related compounds. Multiple harmful algal species often co-occur in the environment, however, emphasizing the need to analyze for the presence of multiple groups of marine and freshwater phycotoxins in environmental samples, e.g., extracts from solid phase adsorption toxin tracking (SPATT). Two methods were developed to screen for 13 phycotoxins (microcystin-RR, -LR, -YR, azaspiracid-1, -2, karlotoxin 3, goniodomin A, brevetoxin-2, yessotoxin, pectenotoxin-2, dinophysistoxin-1, -2, and okadaic acid) in organic SPATT extracts using ultra-performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS) equipped with a trapping dimension (trap) and at-column dilution (ACD). The performance of each compound under 36 combinations of chromatographic conditions was characterized, and two final methods, acidic and basic, were selected based on peak shapes, signal intensities, resolution, and the separation in time of positive and negative MS ionization modes. Injection volumes of up to 1 mL were possible through trap/ACD technology, resulting in limits of detection between 0.001 and 0.05 µg/L across the analytes. Benefits highlighted in this study, beyond the improved detection limits and co-detection of multiple toxin groups, include the ability to inject samples of 100% organic solvent, ensuring analyte stability and streamlining workflow through the elimination of laborious sample preparation steps.
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http://dx.doi.org/10.3390/toxins12050322DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7290987PMC
May 2020

Characterization of Dinophysis spp. (Dinophyceae, Dinophysiales) from the mid-Atlantic region of the United States.

J Phycol 2020 04 10;56(2):404-424. Epub 2020 Feb 10.

Center for Food Safety and Applied Nutrition, Office of Regulatory Science, US Food and Drug Administration, College Park, Maryland, 20740, USA.

Due to the increasing prevalence of Dinophysis spp. and their toxins on every US coast in recent years, the need to identify and monitor for problematic Dinophysis populations has become apparent. Here, we present morphological analyses, using light and scanning electron microscopy, and rDNA sequence analysis, using a ~2-kb sequence of ribosomal ITS1, 5.8S, ITS2, and LSU DNA, of Dinophysis collected in mid-Atlantic estuarine and coastal waters from Virginia to New Jersey to better characterize local populations. In addition, we analyzed for diarrhetic shellfish poisoning (DSP) toxins in water and shellfish samples collected during blooms using liquid-chromatography tandem mass spectrometry and an in vitro protein phosphatase inhibition assay and compared this data to a toxin profile generated from a mid-Atlantic Dinophysis culture. Three distinct morphospecies were documented in mid-Atlantic surface waters: D. acuminata, D. norvegica, and a "small Dinophysis sp." that was morphologically distinct based on multivariate analysis of morphometric data but was genetically consistent with D. acuminata. While mid-Atlantic D. acuminata could not be distinguished from the other species in the D. acuminata-complex (D. ovum from the Gulf of Mexico and D. sacculus from the western Mediterranean Sea) using the molecular markers chosen, it could be distinguished based on morphometrics. Okadaic acid, dinophysistoxin 1, and pectenotoxin 2 were found in filtered water and shellfish samples during Dinophysis blooms in the mid-Atlantic region, as well as in a locally isolated D. acuminata culture. However, DSP toxins exceeded regulatory guidance concentrations only a few times during the study period and only in noncommercial shellfish samples.
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http://dx.doi.org/10.1111/jpy.12966DOI Listing
April 2020

Prey Lysate Enhances Growth and Toxin Production in an Isolate of .

Toxins (Basel) 2019 01 21;11(1). Epub 2019 Jan 21.

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

The physiological and toxicological characteristics of have been increasingly studied in an attempt to better understand and predict diarrhetic shellfish poisoning (DSP) events worldwide. Recent work has identified prey quantity, organic nitrogen, and ammonium as likely contributors to increased growth rates and/or toxicity. Further research is now needed to better understand the interplay between these factors, for example, how inorganic and organic compounds interact with prey and a variety of species and/or strains. In this study, the exudate of ciliate prey and cryptophytes were investigated for an ability to support growth and toxin production in the presence and absence of prey, i.e., during mixotrophic and phototrophic growth respectively. A series of culturing experiments demonstrated that the addition of ciliate lysate led to faster dinoflagellate growth rates (0.25 ± 0.002/d) in predator-prey co-incubations than in treatments containing (1) similar levels of prey but without lysate (0.21 ± 0.003/d), (2) ciliate lysate but no live prey (0.12 ± 0.004/d), or (3) monocultures of without ciliate lysate or live prey (0.01 ± 0.007/d). The addition of ciliate lysate to co-incubations also resulted in maximum toxin quotas and extracellular concentrations of okadaic acid (OA, 0.11 ± 0.01 pg/cell; 1.37 ± 0.10 ng/mL) and dinophysistoxin-1 (DTX1, 0.20 ± 0.02 pg/cell; 1.27 ± 0.10 ng/mL), and significantly greater total DSP toxin concentrations (intracellular + extracellular). Pectenotoxin-2 values, intracellular or extracellular, did not show a clear trend across the treatments. The addition of cryptophyte lysate or whole cells, however, did not support dinoflagellate cell division. Together these data demonstrate that while certain growth was observed when only lysate was added, the benefits to were maximized when ciliate lysate was added with the ciliate inoculum (i.e., during mixotrophic growth). Extrapolating to the field, these culturing studies suggest that the presence of ciliate exudate during co-occurring dinoflagellate-ciliate blooms may indirectly and directly exacerbate abundance and toxigenicity. More research is required, however, to understand what direct or indirect mechanisms control the predator-prey dynamic and what component(s) of ciliate lysate are being utilized by the dinoflagellate or other organisms (e.g., ciliate or bacteria) in the culture if predictive capabilities are to be developed and management strategies created.
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http://dx.doi.org/10.3390/toxins11010057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6356360PMC
January 2019

Effect of ciliate strain, size, and nutritional content on the growth and toxicity of mixotrophic Dinophysis acuminata.

Harmful Algae 2018 09 18;78:95-105. Epub 2018 Aug 18.

Woods Hole Oceanographic Institution, Biology Department, Woods Hole, MA, 02543, USA. Electronic address:

Previous studies indicate differences in bloom magnitude and toxicity between regional populations, and more recently, between geographical isolates of Dinophysis acuminata; however, the factors driving differences in toxicity/toxigenicity between regions/strains have not yet been fully elucidated. Here, the roles of prey strains (i.e., geographical isolates) and their associated attributes (i.e., biovolume and nutritional content) were investigated in the context of growth and production of toxins as a possible explanation for regional variation in toxicity of D. acuminata. The mixotrophic dinoflagellate, D. acuminata, isolated from NE North America (MA, U.S.) was offered a matrix of prey lines in a full factorial design, 1 × 2 × 3; one dinoflagellate strain was fed one of two ciliates, Mesodinium rubrum, isolated from coastal regions of Japan or Spain, which were grown on one of three cryptophytes (Teleaulax/Geminigera clade) isolated from Japan, Spain, or the northeastern USA. Additionally, predator: prey ratios were manipulated to explore effects of the prey's total biovolume on Dinophysis growth or toxin production. These studies revealed that the biovolume and nutritional status of the two ciliates, and less so the cryptophytes, impacted the growth, ingestion rate, and maximum biomass of D. acuminata. The predator's consumption of the larger, more nutritious prey resulted in an elevated growth rate, greater biomass, and increased toxin quotas and total toxin per mL of culture. Grazing on the smaller, less nutritious prey, led to fewer cells in the culture but relatively more toxin exuded from the cells on per cell basis. Once the predator: prey ratios were altered so that an equal biovolume of each ciliate was delivered, the effect of ciliate size was lost, suggesting the predator can compensate for reduced nutrition in the smaller prey item by increasing grazing. While significant ciliate-induced effects were observed on growth and toxin metrics, no major shifts in toxin profile or intracellular toxin quotas were observed that could explain the large regional variations observed between geographical populations of this species.
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http://dx.doi.org/10.1016/j.hal.2018.08.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6178807PMC
September 2018

Impact of nitrogen chemical form on the isotope signature and toxicity of a marine dinoflagellate.

Mar Ecol Prog Ser 2018 23;602:63-76. Epub 2018 Aug 23.

Virginia Institute of Marine Science, Gloucester Point, VA 23062 USA

Despite a global interest in the relationship between harmful algal blooms (HABs) and eutrophication, the impact of natural versus anthropogenic nutrient sources on species composition or toxicity of HABs remains unclear. Stable isotopes are used to identify and track nitrogen (N) sources to water bodies, and thus can be used to ascertain the N source(s) used by the phytoplankton in those systems. To focus this tool for a particular species, the fundamental patterns of N isotope fractionation by that organism must first be understood. While literature is available describing N isotope fractionation by diatoms and coccolithophores, data are lacking regarding dinoflagellates. Here we investigated the effects of N chemical form on isotope fractionation (Δ) and toxin content using isolates of the autotrophic dinoflagellate, in single-N and mixed-N experiments. Growth of exclusively on nitrate (NO ), ammonium (NH ), or urea, resulted in Δ of 2.7±1.4‰, 29±9.3‰, or 0.3±0.1‰, respectively, with the lowest cellular toxicity reported during urea utilization. Cells initially utilized NH and urea when exposed to mixed-N medium, and only utilized NO after NH decreased below 2-4 μM. This pattern of N preference was similar across all N treatments, suggesting that there is no effect of preconditioning on N chemical preference by . In NO and urea-rich environments, the δN of would resemble the source(s) of N utilized, supporting this tool's utility as a tracer of N source(s) facilitating bloom formation, however, caution is advisable in NH rich environments where the large Δ value could lead to misinterpretation of the signal.
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http://dx.doi.org/10.3354/meps12619DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6874107PMC
August 2018

Characterization and comparison of toxin-producing isolates of Dinophysis acuminata from New England and Canada.

J Phycol 2015 Feb 11;51(1):66-81. Epub 2014 Dec 11.

Biology Department and the Woods Hole Center for Oceans and Human Health, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, 02543, USA.

Following the identification of the first toxic isolate of Dinophysis acuminata from the northwestern Atlantic, we conducted detailed investigations into the morphology, phylogeny, physiology, and toxigenicity of three isolates from three sites within the northeastern U.S./Canada region: Eel Pond and Martha's Vineyard, Massachusetts, and the Bay of Fundy. Another isolate, collected from the Gulf of Mexico, was grown under the same light, temperature, and prey conditions for comparison. Despite observed phenotypic heterogeneity, morphometrics and molecular evidence classified the three northwestern Atlantic isolates as D. acuminata Claparède & Lachmann, whereas the isolate from the Gulf of Mexico was morphologically identified as D. cf. ovum. Physiological and toxin analyses supported these classifications, with the three northwestern Atlantic isolates being more similar to each other with respect to growth rate, toxin profile, and diarrhetic shellfish poisoning (DSP) toxin content (okadaic acid + dinophysistoxin 1/cell) than they were to the isolate from the Gulf of Mexico, which had toxin profiles similar to those published for D. cf. ovum F. Schütt. The DSP toxin content, 0.01-1.8 pg okadaic acid (OA) + dinophysistoxin (DTX1) per cell, of the three northwestern Atlantic isolates was low relative to other D. acuminata strains from elsewhere in the world, consistent with the relative scarcity of shellfish harvesting closures due to DSP toxins in the northeastern U.S. and Canada. If this pattern is repeated with the analyses of more geographically and temporally dispersed isolates from the region, it would appear that the risk of significant DSP toxin outbreaks in the northwestern Atlantic is low to moderate. Finally, the morphological, physiological, and toxicological variability within D. acuminata may reflect spatial (and/or temporal) population structure, and suggests that sub-specific resolution may be helpful in characterizing bloom dynamics and predicting toxicity.
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http://dx.doi.org/10.1111/jpy.12251DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5428078PMC
February 2015

Role of dissolved nitrate and phosphate in isolates of and toxin-producing .

Aquat Microb Ecol 2015 24;75(2):169-185. Epub 2015 Jun 24.

Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.

, a producer of toxins associated with diarrhetic shellfish poisoning (DSP) and/or pectenotoxins (PTXs), is a mixotrophic species that requires both ciliate prey and light for growth. Linkages have been described in the literature between natural abundances of the predator and its prey, , and culture experiments have demonstrated that prey, in addition to light, is required for toxin production by ; together these suggest is a critical component for growth and toxicity. However, little is known about the role of dissolved inorganic nutrients on growth or that of toxin-producing . Accordingly, a series of experiments were conducted to investigate the possible uptake of dissolved nitrate and phosphate by 1) starved of prey, 2) feeding on , and 3) grown in nutritionally-modified media. All single-clone or mixed cultures were monitored for dissolved and particulate nutrient levels over the growth cycle, as well as growth rate, biomass, and toxin production when appropriate. did not utilize dissolved nitrate or phosphate in the medium under any nutrient regime tested, i.e., nutrient-enriched and nutrient-reduced, in the absence or presence of prey, or during any growth phase monitored, i.e., exponential and plateau phases. Changes in particulate phosphorus and nitrogen in , were instead, strongly influenced by the consumption of prey, and these levels quickly stabilized once prey were no longer available. , on the other hand, rapidly assimilated dissolved nitrate and phosphate into its particulate nutrient fraction, with maximum uptake rates of 1.38 pmol N/cell/day and 1.63 pmol P/cell/day. While did not benefit directly from the dissolved nitrate and phosphate, its growth (0.37±0.01 day) and toxin production rates for okadaic acid (OA), dinophysistoxin-1 (DTX1) or pectenotoxin-2 (PTX2), 0.1, 0.9 and 2.6 pg /cell/day, respectively, were directly coupled to prey availability. These results suggest that while dissolved nitrate and phosphate do not have a direct effect on toxin production or retention by , these nutrient pools contribute to prey growth and biomass, thereby indirectly influencing blooms and overall toxin in the system.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5055077PMC
http://dx.doi.org/10.3354/ame01757DOI Listing
June 2015

The effects of elevated CO on the growth and toxicity of field populations and cultures of the saxitoxin-producing dinoflagellate, .

Limnol Oceanogr 2015 Jan 31;60(1):198-214. Epub 2014 Dec 31.

Stony Brook University, School of Marine and Atmospheric Sciences, Southampton, NY 11968, USA.

The effects of coastal acidification on the growth and toxicity of the saxitoxin-producing dinoflagellate were examined in culture and ecosystem studies. In culture experiments, strains isolated from Northport Bay NY, USA, and the Bay of Fundy, Canada, grew significantly faster (16 -190%; <0.05) when exposed to elevated levels of pCO (~ 800- 1900μatm) compared to lower levels (~390μatm). Exposure to higher levels of pCO2 also resulted in significant increases (71 - 81%) in total cellular toxicity (fg STX eq. cell) in the Northport Bay strain, while no changes in toxicity were detected in the Bay of Fundy strain. The positive relationship between pCO enhancement and elevated growth was reproducible using natural populations from Northport; densities were significantly and consistently enhanced when natural populations were incubated at 1500 μatm pCO, a value at the upper range of those recorded in Northport Bay, 390 - 1500 µatm. During natural blooms in Northport Bay, pCO concentrations increased over the course of a bloom to more than 1700μatm and were highest in regions with the greatest abundances, suggesting may be further exacerbating acidification or be especially adapted to these extreme, acidified conditions. The co-occurrence of blooms and elevated pCO represents a previously unrecognized, compounding environmental threat to coastal ecosystems. The ability of elevated pCO to enhance the growth and toxicity of indicates that acidification promoted by eutrophication or climate change can intensify these, and perhaps other, harmful algal blooms.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5055070PMC
http://dx.doi.org/10.1002/lno.10012DOI Listing
January 2015

cysts in the Gulf of Maine: long-term time series of abundance and distribution, and linkages to past and future blooms.

Deep Sea Res 2 Top Stud Oceanogr 2014 May;103:6-26

US Geological Survey, Woods Hole, MA 02543 USA.

Here we document cyst abundance and distribution patterns over nine years (1997 and 2004-2011) in the coastal waters of the Gulf of Maine (GOM) and identify linkages between those patterns and several metrics of the severity or magnitude of blooms occurring before and after each autumn cyst survey. We also explore the relative utility of two measures of cyst abundance and demonstrate that GOM cyst counts can be normalized to sediment volume, revealing meaningful patterns equivalent to those determined with dry weight normalization. Cyst concentrations were highly variable spatially. Two distinct seedbeds (defined here as accumulation zones with > 300 cysts cm) are evident, one in the Bay of Fundy (BOF) and one in mid-coast Maine. Overall, seedbed locations remained relatively constant through time, but their area varied 3-4 fold, and total cyst abundance more than 10 fold among years. A major expansion of the mid-coast Maine seedbed occurred in 2009 following an unusually intense bloom with visible red-water conditions, but that feature disappeared by late 2010. The regional system thus has only two seedbeds with the bathymetry, sediment characteristics, currents, biology, and environmental conditions necessary to persist for decades or longer. Strong positive correlations were confirmed between the abundance of cysts in both the 0-1 and the 0-3 cm layers of sediments in autumn and geographic measures of the extent of the bloom that occurred the next year (i.e., → ), such as the length of coastline closed due to shellfish toxicity or the southernmost latitude of shellfish closures. In general, these metrics of bloom geographic extent did not correlate with the number of cysts in sediments following the blooms ( → ). There are, however, significant positive correlations between 0-3 cm cyst abundances and metrics of the preceding bloom that are indicative of bloom intensity or vegetative cell abundance (e.g., cumulative shellfish toxicity, duration of detectable toxicity in shellfish, and bloom termination date). These data suggest that it may be possible to use cyst abundance to empirically forecast the geographic extent of the forthcoming bloom and, conversely, to use other metrics from bloom and toxicity events to forecast the size of the subsequent cyst population as the inoculum for the next year's bloom. This is an important step towards understanding the excystment/encystment cycle in bloom dynamics while also augmenting our predictive capability for this HAB-forming species in the GOM.
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http://dx.doi.org/10.1016/j.dsr2.2013.10.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4085992PMC
May 2014

Toxin profiles of five geographical isolates of Dinophysis spp. from North and South America.

Toxicon 2011 Feb 10;57(2):275-87. Epub 2010 Dec 10.

U.S. Food and Drug Administration, Gulf Coast Seafood Laboratory, 1 Iberville Drive, Dauphin Island, AL 36528, USA.

Marine dinoflagellates of the genus Dinophysis can produce toxins of the okadaic acid (OA) and pectenotoxin (PTX) groups. These lipophilic toxins accumulate in filter-feeding shellfish and cause an illness in consumers called diarrhetic shellfish poisoning (DSP). In 2008, a bloom of Dinophysis led to the closure of shellfish harvesting areas along the Texas coast, one of the first DSP-related closures in the U.S. This event resulted in a broad study of toxin production in isolates of Dinophysis spp. from U.S. waters. In the present study, we compared toxin profiles in geographical isolates of Dinophysis collected in the U.S. (Eel Pond, Woods Hole MA; Martha's Vineyard, MA; and Port Aransas Bay, Texas), and in those from Canada (Blacks Harbour, Bay of Fundy) and Chile (Reloncavi Estuary), when cultured in the laboratory under the same conditions. For each isolate, the mitochondrial cox1 gene was sequenced to assist in species identification. Strains from the northeastern U.S. and Canada were all assigned to Dinophysis acuminata, while those from Chile and Texas were most likely within the D. acuminata complex whereas precise species designation could not be made with this marker. Toxins were detected in all Dinophysis isolates and each isolate had a different profile. Toxin profiles of isolates from Eel Pond, Martha's Vineyard, and Bay of Fundy were most similar, in that they all contained OA, DTX1, and PTX2. The Eel Pond isolate also contained OA-D8 and DTX1-D7, and low levels (unconfirmed structurally) of DTX1-D8 and DTX1-D9. D. acuminata from Martha's Vineyard produced DTX1-D7, along with OA, DTX1, and PTX2, as identified in both the cells and the culture medium. D. acuminata from the Bay of Fundy produced DTX1 and PTX2, as found in both cells and culture medium, while only trace amounts of OA were detected in the medium. The Dinophysis strain from Texas only produced OA, and the one from Chile only PTX2, as confirmed in both cells and culture medium.
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http://dx.doi.org/10.1016/j.toxicon.2010.12.002DOI Listing
February 2011

Possible mechanism for the foodweb transfer of covalently bound microcystins.

Ecotoxicol Environ Saf 2010 Jul 13;73(5):757-61. Epub 2010 Jan 13.

Department of Environmental and Forest Biology, State University of New York, Syracuse, College of Environmental Science and Forestry, Syracuse, NY 13210, USA.

Microcystins (MCs) are cyanobacterial toxins that inhibit protein phosphatases 1 and 2A (PP1, PP2A) within an animal through both reversible and covalent interactions. Only MCs that have accumulated in animal tissue in reversible interactions are currently considered when estimating risk to higher trophic levels and humans through food web exposure. However, the majority of MCs is likely covalently bound to target proteins in tissues and these MCs are not quantified or included in these assessments. These covalently bound MCs may be made bioavailable in the digestive system of a consumer through the digestion of their attached protein phosphatase. Three common digestive enzymes, pepsin, chymotrypsin, and trypsin, did not digest cyclic MC-LR and MC-LY, but were very active against a control peptide with typical linkages and standard amino acids in "L" conformation, supporting the possibility for MC-peptide formation during gut passage. To test if digestion products could be biologically active in the consumer, four predicted MC-peptides were synthesized and assayed for activity against PP1 by the protein phosphatase inhibition assay (PPIA). All four MC-peptides were active against PP1 and comparably half (58%) as inhibitory as the parent toxin. This in vitro study demonstrated that MCs covalently bound to proteins may represent a reservoir of potential toxicity for consumers.
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http://dx.doi.org/10.1016/j.ecoenv.2009.12.003DOI Listing
July 2010

Standardization of microcystin extraction from fish tissues: a novel internal standard as a surrogate for polar and non-polar variants.

Toxicon 2009 Feb 28;53(2):238-45. Epub 2008 Nov 28.

SUNY Syracuse, College of Environmental Science and Forestry, Department of Environmental and Forest Biology, 1 Forestry Drive, Syracuse, NY 13210, USA.

Microcystins (MCs), a class of potent liver/hepatopancreatic toxins produced by numerous species of freshwater cyanobacteria, are well known for their toxic effects on aquatic organisms and humans. The extraction efficiencies of MCs can vary greatly as a result of matrix differences and/or differences in the extraction solvents, techniques, and clean-up steps utilized. Here we report the preparation of a unique internal standard, (S-hydroxypropyl-cys7)microcystin-LR (thiol-LR), with a mass different than any known MCs, which can be spiked into field samples and quantified via HPLC-MS along with endogenous MCs. Thiol-LR is modified at the Mdha residue, and therefore, provides an accurate measure of only free MCs that are not covalently bound to endogenous thiols in the matrix. The internal standard proved to be a good surrogate for MC-RR, -LR, and -LA in fish liver tissue. In fish muscle tissue, thiol-LR was a good surrogate for polar variants, MC-RR and -LR, but was less representative of the non-polar variant, MC-LA. Coupling of the internal standard (8 microg/g ww tissue) with HPLC-MS detection will standardize the quantification of free microcystins across species, tissue types, and extraction methods, making the estimation of exposure risk more reliable.
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http://dx.doi.org/10.1016/j.toxicon.2008.11.007DOI Listing
February 2009

Toxicity of microcystin-LR, a cyanobacterial toxin, to multiple life stages of the burrowing mayfly, Hexagenia, and possible implications for recruitment.

Environ Toxicol 2008 Aug;23(4):499-506

Department of Environmental and Forest Biology, SUNY Syracuse, College of Environmental Science and Forestry, 1 Forestry Drive, Syracuse, New York 13210, USA.

Burrowing mayflies, genus Hexagenia, were extirpated from the major water bodies of North America in the early 1950s, paralleling an increase in eutrophication and organic pollution, and a decrease in dissolved oxygen concentrations. Burrowing mayflies recolonized the western basin of Lake Erie, but remain absent in other former habitats such as Oneida Lake, New York. Eutrophication is commonly associated with a shift in the phytoplankton community toward dominance by cyanobacteria, and therefore, one class of cyanobacterial toxins, microcystins, were investigated as a contributing factor to Hexagenia's eradication or as an impediment to recolonization. Laboratory experiments were conducted to determine if microcystin-LR (MC-LR) produced negative effects on Hexagenia at three points within its life cycle: egg, hatchling nymph (<24-h old, <1 mm total length), and pre-emergence nymph (>17 mm). Treatment concentrations ranged from the guideline set by the World Health Organization for drinking water (0.001 microg mL(-1)) to 0.1 microg mL(-1) for the egg experiment and 10 microg mL(-1) for the nymph trials. Eggs showed a delay in hatching and an altered distribution of hatching over the study period when submerged in 0.1 microg mL(-1) MC-LR (an elevated concentration representative of bloom scum). The 72-h (1.1 microg mL(-1)) and 96-h (0.049 microg mL(-1)) LC(50) values for hatchling nymphs exceeded typical bloom concentrations of North American lakes, (0.01 microg mL(-1)). Large nymphs were more tolerant of the toxin, as indicated by 100% survival over seven days exposure to 10 microg mL(-1), suggesting older larvae can withstand brief encounters with high microcystin levels for at least short periods of time. The sensitivity of young nymphs and eggs to MC-LR may have implications for the recruitment of the genus in water bodies with persistent summer cyanobacterial blooms.
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http://dx.doi.org/10.1002/tox.20369DOI Listing
August 2008

Foodweb transfer, accumulation, and depuration of microcystins, a cyanobacterial toxin, in pumpkinseed sunfish (Lepomis gibbosus).

Toxicon 2006 Oct 11;48(5):580-9. Epub 2006 Jul 11.

Faculty of Environmental and Forest Biology, State University of New York, Syracuse, College of Environmental Science and Forestry, 1 Forestry Drive, Syracuse, NY 13210, USA.

Zooplankton accumulate microcystins (MC), a potent cyanobacteria toxin, and therefore may act as vectors of the toxin up the aquatic food web; however this transfer has not yet been quantified. In addition there is a lack of information regarding fish's ability to metabolize MC when administered a low dose over a longer period of time. We monitored MC concentrations in three levels of an aquatic food web: phytoplankton, zooplankton, and sunfish (Lepomis gibbosus). Bosmina appeared to be both a major accumulator of MC in zooplankton and the major vector of MC to sunfish. In an accumulation experiment, sunfish were brought into the laboratory and fed MC-rich zooplankton pellets (50 ng MC kg(-1)d(-1)) for 9 days. Zooplankton directly transferred MC to sunfish, resulting in liver and muscle tissue accumulation. However, after 6 days of accumulation fish significantly decreased concentrations in their liver and muscle tissue, indicating the induction of a detoxification and excretion pathway. Sunfish retained MC in their liver and muscle tissue, showing no significant changes in toxin concentration over 2 weeks of fasted depuration.
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http://dx.doi.org/10.1016/j.toxicon.2006.07.009DOI Listing
October 2006
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