Publications by authors named "Donald M Anderson"

95 Publications

Effects of soluble organics on the settling rate of modified clay and development of improved clay formulations for harmful algal bloom control.

Environ Pollut 2021 Aug 13;289:117964. Epub 2021 Aug 13.

CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China; Functional Laboratory of Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China; University of Chinese Academy of Sciences, Beijing, 100049, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, 266071, PR China.

For many years, the dispersal of modified clay (MC) has been used to control harmful algal blooms (HABs) in coastal waters of China. MC flocculation efficiency can be influenced by many factors in variable and complex natural environments, including high concentrations of dissolved organic matter (DOM) in the water to be treated. Since many HABs occur in nearshore waters where DOM concentrations are high, this is a significant problem that requires urgent attention. This study involved the use of humic acid as a representative form of DOM to study the influence of organic matter on the MC flocculation process. At high concentrations, humic acid was adsorbed onto MC particles, resulting in a decrease in surface potential and an increase in electrostatic repulsion between the clay particles; this decreased the MC settling rate and increased the water clarification time. Flocs were characterized by their relatively small particle size, high particle concentration, and low collision efficiency, which together resulted in slow clarification of the water after MC spraying. Based on the mechanism of the DOM-MC interaction and combined with the Derjaguin-Landau-Verwey-Overbeek theory and theoretical considerations of clay surface modification, the "ionic atmosphere compression" method was used to improve MC flocculation efficiency in high-organic water. This method increased the ionic strength of the clay stock solution by adding salt, thereby compressing the ionic atmosphere of MC particles and lowering the potential barrier, allowing the MC particles in the treated water to flocculate rapidly and form large flocs, followed by further floc growth and rapid settling via differential sedimentation. The settling rate of MCs improved by a factor of two and the removal efficiency of the HAB cells increased by 7-28%. This study provides important baseline information that will extend the application of MC to HAB control in water bodies with high organic loadings.
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http://dx.doi.org/10.1016/j.envpol.2021.117964DOI Listing
August 2021

Asynchrony of spp. Abundance and Toxicity in the U.S. Virgin Islands: Implications for Monitoring and Management of Ciguatera.

Toxins (Basel) 2021 06 10;13(6). Epub 2021 Jun 10.

School of Marine and Environmental Sciences, University of South Alabama, Mobile, Alabama, AL 36688, USA.

Ciguatera poisoning (CP) poses a significant threat to ecosystem services and fishery resources in coastal communities. The CP-causative ciguatoxins (CTXs) are produced by benthic dinoflagellates including and spp., and enter reef food webs via grazing on macroalgal substrates. In this study, we report on a 3-year monthly time series in St. Thomas, US Virgin Islands where spp. abundance and Caribbean-CTX toxicity in benthic samples were compared to key environmental factors, including temperature, salinity, nutrients, benthic cover, and physical data. We found that peak abundance occurred in summer while CTX-specific toxicity peaked in cooler months (February-May) when the mean water temperatures were approximately 26-28 °C. These trends were most evident at deeper offshore sites where macroalgal cover was highest year-round. Other environmental parameters were not correlated with the CTX variability observed over time. The asynchrony between spp. abundance and toxicity reflects potential differences in toxin cell quotas among species with concomitant variability in their abundances throughout the year. These results have significant implications for monitoring and management of benthic harmful algal blooms and highlights potential seasonal and highly-localized pulses in reef toxin loads that may be transferred to higher trophic levels.
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http://dx.doi.org/10.3390/toxins13060413DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8230442PMC
June 2021

Evaluation of 24-h screen deployments as a standardized platform to monitor Gambierdiscus populations in the Florida Keys and U.S. Virgin Islands.

Harmful Algae 2021 03 13;103:101998. Epub 2021 Feb 13.

Biology Department, MS #32, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.

Anchored mesh screens have been suggested as a standardized approach to monitor the cell abundances of epiphytic dinoflagellates in benthic habitats, including toxigenic members of the Gambierdiscus genus responsible for ciguatera poisoning (CP). Here we deployed screens for 24h at eight sites in the Florida Keys and St. Thomas (US Virgin Islands) to evaluate their performance relative to the traditional method of assessing Gambierdiscus abundance in which cell counts are normalized to wet weight of host algae. The 30-month study (April 2013 - August 2015) involved monthly sampling at sites where screens were suspended at near-bottom locations for a 24h period and retrieved, with concurrent collections of macrophytes; including Halimeda, Laurencia, and Thalassia in the Florida Keys, and Dictyota in both regions. Gambierdiscus cells were identified and enumerated in the screen and macrophyte samples, and several regression techniques were evaluated (linear regression using untransformed and log-transformed data; negative binomial distribution (NBD) regression) to determine how well the screen-derived data could estimate algal cell concentrations on the host algae. In all cases, the NBD models performed the best based on Akaike Information Criteria values, although 38% of the regressions were not statistically-significant, including all of the St. Thomas sites. The r values were all < 0.75 and averaged 0.36, indicating relatively poor fit of the screen data. False negative results (regression models underestimating actual cell abundances) were common occurrences, ranging from 5 to 74% of the scenarios tested. In summary, these results indicate that 24h screen deployments do not appear to be consistent in all situations. Caution is therefore needed when considering 24h screens as a standardized monitoring approach for quantifying Gambierdiscus population dynamics across geography and ecosystems. Furthermore, neutral (artificial) substrates may not adequately capture either the host preference or palatability that likely influence the initial vector of toxin incorporation in the food web via herbivory on these macrophytes.
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http://dx.doi.org/10.1016/j.hal.2021.101998DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8119931PMC
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

Molecular Identification and Toxin Analysis of spp. in the Beibu Gulf: First Report of Toxic in Chinese Coastal Waters.

Toxins (Basel) 2021 02 18;13(2). Epub 2021 Feb 18.

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

The frequency of harmful algal blooms (HABs) has increased in China in recent years. Information about harmful dinoflagellates and paralytic shellfish toxins (PSTs) is still limited in China, especially in the Beibu Gulf, where PSTs in shellfish have exceeded food safety guidelines on multiple occasions. To explore the nature of the threat from PSTs in the region, eight strains were isolated from waters of the Beibu Gulf and examined using phylogenetic analyses of large subunit (LSU) rDNA, small subunit (SSU) rDNA, and internal transcribed spacer (ITS) sequences. Their toxin composition profiles were also determined using liquid chromatography-tandem mass spectrometry (LC-MS/MS). All eight strains clustered in the phylogenetic tree with , , and from other locations, forming three well-resolved groups. The intraspecific genetic distances of the three species were significantly smaller than interspecific genetic distances for species. Beibu Gulf isolates were therefore classified as , , and . No PSTs were identified in , but low levels of gonyautoxins (GTXs) 1 to 5, and saxitoxin (STX) were detected in (a total of 4.60 fmol/cell). The extremely low level of toxicity is inconsistent with PST detection above regulatory levels on multiple occasions within the Beibu Gulf, suggesting that higher toxicity strains may occur in those waters, but were unsampled. Other explanations including biotransformation of PSTs in shellfish and the presence of other PST-producing algae are also suggested. Understanding the toxicity and phylogeny of species provides foundational data for the protection of public health in the Beibu Gulf region and the mitigation of HAB events.
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http://dx.doi.org/10.3390/toxins13020161DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7922158PMC
February 2021

Development of fluorescence in situ hybridization (FISH) probes to detect and enumerate Gambierdiscus species.

Harmful Algae 2021 01 6;101:101914. Epub 2021 Jan 6.

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

Ciguatera poisoning (CP) is a syndrome caused by the bioaccumulation of lipophilic ciguatoxins in coral reef fish and invertebrates, and their subsequent consumption by humans. These phycotoxins are produced by Gambierdiscus spp., tropical epiphytic dinoflagellates that live on a variety of macrophytes, as well as on dead corals and sand. Recent taxonomic studies have identified novel diversity within the Gambierdiscus genus, with at least 18 species and several sub-groups now identified, many of which co-occur and differ significantly in toxicity. The ability to accurately and quickly distinguish Gambierdiscus species in field samples and determine community composition and abundance is central to assessing CP risk, yet most Gambierdiscus species are indistinguishable using light microscopy, and other enumeration methods are semi-quantitative. In order to investigate the spatial and temporal dynamics of Gambierdiscus species and community toxicity, new tools for species identification and enumeration in field samples are needed. Here, fluorescence in situ hybridization (FISH) probes were designed for seven species commonly found in the Caribbean Sea and Pacific Ocean, permitting their enumeration in field samples using epifluorescence microscopy. This technique enables the assessment of community composition and accurate determination of cell abundances of individual species. Molecular probes detecting G. australes, G. belizeanus, G. caribaeus, G. carolinianus, G. carpenteri, and the G. silvae/G. polynesiensis clade were designed using alignments of large subunit ribosomal RNA (rRNA) sequences. These probes were tested for specificity and cross-reactivity through experiments in which field samples were spiked with known concentrations of Gambierdiscus cultures, and analyzed to confirm that Gambierdiscus can be successfully detected and enumerated by FISH in the presence of detritus and other organisms. These probes were then used to characterize Gambierdiscus community structure in field samples collected from the Florida Keys and Hawai'i, USA. The probes revealed the co-occurrence of multiple species at each location. Time-series FISH analyses of samples collected from the Florida Keys quantified seasonal shifts in community composition as well as fluctuations in overall Gambierdiscus cell abundance. Application of species-specific FISH probes provides a powerful new tool to those seeking to target individual Gambierdiscus species, including significant toxin-producers, in field populations. Moving forward, analysis of Gambierdiscus community composition across multiple environments and over time will also allow species dynamics to be linked to environmental parameters, improving our ability to understand and manage the current and changing risks of CP worldwide.
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http://dx.doi.org/10.1016/j.hal.2020.101914DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8016406PMC
January 2021

Disentangling the environmental processes responsible for the world's largest farmed fish-killing harmful algal bloom: Chile, 2016.

Sci Total Environ 2021 Apr 25;766:144383. Epub 2020 Dec 25.

Institute for Marine and Antarctic Studies (IMAS), University of Tasmania, Australia.

The dictyochophyte microalga Pseudochattonella verruculosa was responsible for the largest farmed fish mortality ever recorded in the world, with losses for the Chilean salmon industry amounting to US$ 800 M in austral summer 2016. Super-scale climatic anomalies resulted in strong vertical water column stratification that stimulated development of a dynamic P. verruculosa thin layer (up to 38 μg chl a L) for several weeks in Reloncaví Sound. Hydrodynamic modeling (MIKE 3D) indicated that the Sound had extremely low flushing rates (between 121 and 200 days) in summer 2016. Reported algal cell densities of 7000-20,000 cells mL generated respiratory distress in fish that was unlikely due to low dissolved oxygen (permanently >4 mg L). Histological examination of salmon showed that gills were the most affected organ with significant tissue damage and circulatory disorders. It is possible that some of this damage was due to a diatom bloom that preceded the Pseudochattonella event, thereby rendering the fish more susceptible to Pseudochattonella. No correlation between magnitude of fish mortality and algal cell abundance nor fish age was evident. Algal cultures revealed rapid growth rates and high cell densities (up to 600,000 cells mL), as well as highly complex life cycle stages that can be easily overlooked in monitoring programs. In cell-based bioassays, Chilean P. verruculosa was only toxic to the RTgill-W1 cell line following exposures to high cell densities of lysed cells (>100,000 cells mL). Fatty acid profiles of a cultured strain showed elevated concentrations of potentially ichthyotoxic, long-chain polyunsaturated fatty acids (PUFAs) (69.7% ± 1.8%)- stearidonic (SDA, 18:4ω3-28.9%), and docosahexaenoic acid (DHA, 22:6ω3-22.3%), suggesting that lipid peroxidation may help to explain the mortalities, though superoxide production by Pseudochattonella was low (< 0.21 ± 0.19 pmol O cell h). It therefore remains unknown what the mechanisms of salmon mortality were during the Pseudochattonella bloom. Multiple mitigation strategies were used by salmon farmers during the event, with only delayed seeding of juvenile fish into the cages and towing of cages to sanctuary sites being effective. Airlift pumping, used effectively against other fish-killing HABs in the US and Canada was not effective, perhaps because it brought subsurface layers of Pseudochattonella to the surface, or and it also may have lysed the fragile cells, rendering them more lethal. The present study highlights knowledge gaps and inefficiency of contingency plans by the fish farming industry to overcome future fish-killing algal blooms under future climate change scenarios. The use of new technologies based on molecular methods for species detection, good farm practices by fish farms, and possible mitigation strategies are discussed.
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http://dx.doi.org/10.1016/j.scitotenv.2020.144383DOI Listing
April 2021

Human Health and Ocean Pollution.

Ann Glob Health 2020 12 3;86(1):151. Epub 2020 Dec 3.

Nigerian Institute for Medical Research, Lagos, NG.

Background: Pollution - unwanted waste released to air, water, and land by human activity - is the largest environmental cause of disease in the world today. It is responsible for an estimated nine million premature deaths per year, enormous economic losses, erosion of human capital, and degradation of ecosystems. Ocean pollution is an important, but insufficiently recognized and inadequately controlled component of global pollution. It poses serious threats to human health and well-being. The nature and magnitude of these impacts are only beginning to be understood.

Goals: (1) Broadly examine the known and potential impacts of ocean pollution on human health. (2) Inform policy makers, government leaders, international organizations, civil society, and the global public of these threats. (3) Propose priorities for interventions to control and prevent pollution of the seas and safeguard human health.

Methods: Topic-focused reviews that examine the effects of ocean pollution on human health, identify gaps in knowledge, project future trends, and offer evidence-based guidance for effective intervention.

Environmental Findings: Pollution of the oceans is widespread, worsening, and in most countries poorly controlled. It is a complex mixture of toxic metals, plastics, manufactured chemicals, petroleum, urban and industrial wastes, pesticides, fertilizers, pharmaceutical chemicals, agricultural runoff, and sewage. More than 80% arises from land-based sources. It reaches the oceans through rivers, runoff, atmospheric deposition and direct discharges. It is often heaviest near the coasts and most highly concentrated along the coasts of low- and middle-income countries. Plastic is a rapidly increasing and highly visible component of ocean pollution, and an estimated 10 million metric tons of plastic waste enter the seas each year. Mercury is the metal pollutant of greatest concern in the oceans; it is released from two main sources - coal combustion and small-scale gold mining. Global spread of industrialized agriculture with increasing use of chemical fertilizer leads to extension of Harmful Algal Blooms (HABs) to previously unaffected regions. Chemical pollutants are ubiquitous and contaminate seas and marine organisms from the high Arctic to the abyssal depths.

Ecosystem Findings: Ocean pollution has multiple negative impacts on marine ecosystems, and these impacts are exacerbated by global climate change. Petroleum-based pollutants reduce photosynthesis in marine microorganisms that generate oxygen. Increasing absorption of carbon dioxide into the seas causes ocean acidification, which destroys coral reefs, impairs shellfish development, dissolves calcium-containing microorganisms at the base of the marine food web, and increases the toxicity of some pollutants. Plastic pollution threatens marine mammals, fish, and seabirds and accumulates in large mid-ocean gyres. It breaks down into microplastic and nanoplastic particles containing multiple manufactured chemicals that can enter the tissues of marine organisms, including species consumed by humans. Industrial releases, runoff, and sewage increase frequency and severity of HABs, bacterial pollution, and anti-microbial resistance. Pollution and sea surface warming are triggering poleward migration of dangerous pathogens such as the species. Industrial discharges, pharmaceutical wastes, pesticides, and sewage contribute to global declines in fish stocks.

Human Health Findings: Methylmercury and PCBs are the ocean pollutants whose human health effects are best understood. Exposures of infants to these pollutants through maternal consumption of contaminated seafood can damage developing brains, reduce IQ and increase children's risks for autism, ADHD and learning disorders. Adult exposures to methylmercury increase risks for cardiovascular disease and dementia. Manufactured chemicals - phthalates, bisphenol A, flame retardants, and perfluorinated chemicals, many of them released into the seas from plastic waste - can disrupt endocrine signaling, reduce male fertility, damage the nervous system, and increase risk of cancer. HABs produce potent toxins that accumulate in fish and shellfish. When ingested, these toxins can cause severe neurological impairment and rapid death. HAB toxins can also become airborne and cause respiratory disease. Pathogenic marine bacteria cause gastrointestinal diseases and deep wound infections. With climate change and increasing pollution, risk is high that infections, including cholera, will increase in frequency and extend to new areas. All of the health impacts of ocean pollution fall disproportionately on vulnerable populations in the Global South - environmental injustice on a planetary scale.

Conclusions: Ocean pollution is a global problem. It arises from multiple sources and crosses national boundaries. It is the consequence of reckless, shortsighted, and unsustainable exploitation of the earth's resources. It endangers marine ecosystems. It impedes the production of atmospheric oxygen. Its threats to human health are great and growing, but still incompletely understood. Its economic costs are only beginning to be counted.Ocean pollution can be prevented. Like all forms of pollution, ocean pollution can be controlled by deploying data-driven strategies based on law, policy, technology, and enforcement that target priority pollution sources. Many countries have used these tools to control air and water pollution and are now applying them to ocean pollution. Successes achieved to date demonstrate that broader control is feasible. Heavily polluted harbors have been cleaned, estuaries rejuvenated, and coral reefs restored.Prevention of ocean pollution creates many benefits. It boosts economies, increases tourism, helps restore fisheries, and improves human health and well-being. It advances the Sustainable Development Goals (SDG). These benefits will last for centuries.

Recommendations: World leaders who recognize the gravity of ocean pollution, acknowledge its growing dangers, engage civil society and the global public, and take bold, evidence-based action to stop pollution at source will be critical to preventing ocean pollution and safeguarding human health.Prevention of pollution from land-based sources is key. Eliminating coal combustion and banning all uses of mercury will reduce mercury pollution. Bans on single-use plastic and better management of plastic waste reduce plastic pollution. Bans on persistent organic pollutants (POPs) have reduced pollution by PCBs and DDT. Control of industrial discharges, treatment of sewage, and reduced applications of fertilizers have mitigated coastal pollution and are reducing frequency of HABs. National, regional and international marine pollution control programs that are adequately funded and backed by strong enforcement have been shown to be effective. Robust monitoring is essential to track progress.Further interventions that hold great promise include wide-scale transition to renewable fuels; transition to a circular economy that creates little waste and focuses on equity rather than on endless growth; embracing the principles of green chemistry; and building scientific capacity in all countries.Designation of Marine Protected Areas (MPAs) will safeguard critical ecosystems, protect vulnerable fish stocks, and enhance human health and well-being. Creation of MPAs is an important manifestation of national and international commitment to protecting the health of the seas.
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http://dx.doi.org/10.5334/aogh.2831DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7731724PMC
December 2020

Wind-driven development and transport of blooms along the coast of Fujian, China.

Reg Stud Mar Sci 2020 Sep 12;39. Epub 2020 Aug 12.

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

is a cosmopolitan, bloom-forming dinoflagellate known to produce a suite of potent paralytic shellfish poisoning (PSP) toxins. Here, we revisit two major blooms of along the Fujianese Coast, China, in 2017 and 2018. The impact area of the 2017 bloom was larger than that of the 2018 event. Field sampling and remote satellite sensing revealed that alongshore transport driven by the southwest wind, as well as physical accumulation driven by the northeast wind, played important roles in the development and distribution of the two bloom events. The relationship between wind-induced hydrodynamic conditions and the unprecedented HAB events established in this study adds greatly to our understanding of algal bloom dynamics along the Fujianese coast. These results improve our ability to detect, track, and forecast blooms, thereby potentially minimizing the negative impacts of future HAB events.
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http://dx.doi.org/10.1016/j.rsma.2020.101397DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7685303PMC
September 2020

Morphological and phylogenetic data do not support the split of Alexandrium into four genera.

Harmful Algae 2020 09 18;98:101902. Epub 2020 Sep 18.

MARBEC, Université de Montpellier, CNRS, Ifremer, IRD, Montpellier, France.

A recently published study analyzed the phylogenetic relationship between the genera Centrodinium and Alexandrium, confirming an earlier publication showing the genus Alexandrium as paraphyletic. This most recent manuscript retained the genus Alexandrium, introduced a new genus Episemicolon, resurrected two genera, Gessnerium and Protogonyaulax, and stated that: "The polyphyly [sic] of Alexandrium is solved with the split into four genera". However, these reintroduced taxa were not based on monophyletic groups. Therefore this work, if accepted, would result in replacing a single paraphyletic taxon with several non-monophyletic ones. The morphological data presented for genus characterization also do not convincingly support taxa delimitations. The combination of weak molecular phylogenetics and the lack of diagnostic traits (i.e., autapomorphies) render the applicability of the concept of limited use. The proposal to split the genus Alexandrium on the basis of our current knowledge is rejected herein. The aim here is not to present an alternative analysis and revision, but to maintain Alexandrium. A better constructed and more phylogenetically accurate revision can and should wait until more complete evidence becomes available and there is a strong reason to revise the genus Alexandrium. The reasons are explained in detail by a review of the available molecular and morphological data for species of the genera Alexandrium and Centrodinium. In addition, cyst morphology and chemotaxonomy are discussed, and the need for integrative taxonomy is highlighted.
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http://dx.doi.org/10.1016/j.hal.2020.101902DOI Listing
September 2020

Role of C carbon fixation in Ulva prolifera, the macroalga responsible for the world's largest green tides.

Commun Biol 2020 09 7;3(1):494. Epub 2020 Sep 7.

State Key Laboratory of Estuarine and Coastal Research, Institute of Eco-Chongming, East China Normal University, Shanghai, 200062, China.

Most marine algae preferentially assimilate CO via the Calvin-Benson Cycle (C) and catalyze HCO dehydration via carbonic anhydrase (CA) as a CO-compensatory mechanism, but certain species utilize the Hatch-Slack Cycle (C) to enhance photosynthesis. The occurrence and importance of the C pathway remains uncertain, however. Here, we demonstrate that carbon fixation in Ulva prolifera, a species responsible for massive green tides, involves a combination of C and C pathways and a CA-supported HCO mechanism. Analysis of CA and key C and C enzymes, and subsequent analysis of δC photosynthetic products showed that the species assimilates CO predominately via the C pathway, uses HCO via the CA mechanism at low CO levels, and takes advantage of high irradiance using the C pathway. This active and multi-faceted carbon acquisition strategy is advantageous for the formation of massive blooms, as thick floating mats are subject to intense surface irradiance and CO limitation.
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http://dx.doi.org/10.1038/s42003-020-01225-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7477558PMC
September 2020

Cyst-forming dinoflagellates in a warming climate.

Harmful Algae 2020 01 20;91:101728. Epub 2019 Dec 20.

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

Many phytoplankton species, including many harmful algal bloom (HAB) species, survive long periods between blooms through formation of benthic resting stages. Because they are crucial to the persistence of these species and the initiation of new blooms, the physiology of benthic stages must be considered to accurately predict responses to climate warming and associated environmental changes. The benthic stages of dinoflagellates, called resting cysts, germinate in response to the combination of favorable temperature, oxygen-availability, and release from dormancy. The latter is a mechanism that prevents germination even when oxygen and temperature conditions are favorable. Here, evidence of temperature-mediated control of dormancy duration from the dinoflagellates Alexandrium catenella and Pyrodinium bahamense-two HAB species that cause paralytic shellfish poisoning (PSP)-is reviewed and presented alongside new evidence of complementary, temperature-based control of cyst quiescence (the state in which cysts germinate on exposure to favorable conditions). Interaction of the two temperature-based mechanisms with climate is explored through a simple model parameterized using results from recent experiments with A. catenella. Simulations demonstrate the importance of seasonal temperature cycles for the synchronization of cysts' release from dormancy and are consistent with biogeography-based inferences that A. catenella is more tolerant of warming in habitats that experience a larger range of seasonal temperature variation (i.e., have higher temperature seasonality). Temperature seasonality is much greater in shallow, long-residence time habitats than in deep, open-water ones. As warming shifts species' ranges, cyst beds may persist longer in more seasonally variable, shallow inshore habitats than in deep offshore ones, promoting HABs that are more localized and commence earlier each year. Recent field investigations of A. catenella also point to the importance of new cyst formation as a factor triggering bloom termination through mass sexual induction. In areas where temperature seasonality restricts the flux of new swimming cells (germlings) to narrow temporal windows, warming is unlikely to promote longer and more intense HAB impacts-even when water column conditions would otherwise promote prolonged bloom development. Many species likely have a strong drive to sexually differentiate and produce new cysts once concentrations reach levels that are conducive to new cyst formation. This phenomenon can impose a limit to bloom intensification and suggests an important role for cyst bed quiescence in determining the duration of HAB risk periods.
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http://dx.doi.org/10.1016/j.hal.2019.101728DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7189352PMC
January 2020

Cell cycle regulation of the mixotrophic dinoflagellate Dinophysis acuminata: Growth, photosynthetic efficiency and toxin production.

Harmful Algae 2019 11 11;89:101672. Epub 2019 Oct 11.

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

The mixotrophic dinoflagellate Dinophysis acuminata is a widely distributed diarrhetic shellfish poisoning (DSP) producer. Toxin variability of Dinophysis spp. has been well studied, but little is known of the manner in which toxin production is regulated throughout the cell cycle in these species, in part due to their mixotrophic characteristics. Therefore, an experiment was conducted to investigate cell cycle regulation of growth, photosynthetic efficiency, and toxin production in D. acuminata. First, a three-step synchronization approach, termed "starvation-feeding-dark", was used to achieve a high degree of synchrony of Dinophysis cells by starving the cells for 2 weeks, feeding them once, and then placing them in darkness for 58 h. The synchronized cells started DNA synthesis (S phase) 10 h after being released into the light, initiated G2 growth stage eight hours later, and completed mitosis (M phase) 2 h before lights were turned on. The toxin content of three dominant toxins, okadaic acid (OA), dinophysistoxin-1 (DTX1) and pectenotoxin-2 (PTX2), followed a common pattern of increasing in G1 phase, decreasing on entry into the S phase, then increasing again in S phase and decreasing in M phase during the diel cell cycle. Specific toxin production rates were positive throughout the G1 and S phases, but negative during the transition from G1 to S phase and late in M phase, the latter reflecting cell division. All toxins were initially induced by the light and positively correlated with the percentage of cells in S phase, indicating that biosynthesis of Dinophysis toxins might be under circadian regulation and be most active during DNA synthesis.
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http://dx.doi.org/10.1016/j.hal.2019.101672DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6914227PMC
November 2019

Evaluation of sxtA and rDNA qPCR assays through monitoring of an inshore bloom of Alexandrium catenella Group 1.

Sci Rep 2019 10 10;9(1):14532. Epub 2019 Oct 10.

Woods Hole Oceanographic Institution, MS # 32, 266 Woods Hole Road, Woods Hole, Massachusetts, 02543, United States.

Alexandrium catenella (formerly A. tamarense Group 1, or A. fundyense) is the leading cause of Paralytic Shellfish Poisoning in North and South America, Europe, Africa, Australia and Asia. The quantification of A.catenella via sxtA, a gene involved in Paralytic Shellfish Toxin synthesis, may be a promising approach, but has not been evaluated in situ on blooms of A. catenella, in which cell abundances may vary from not detectable to in the order of 10 cells L. In this study, we compared sxtA assay performance to a qPCR assay targeted to a species-specific region of ribosomal DNA (rDNA) and an established fluorescent in situ hybridization (FISH) microscopy method. Passing-Bablok regression analyses revealed the sxtA assay to overestimate abundances when <5 cell equivalents A. catenella DNA were analysed, but otherwise was closer to microscopy estimates than the rDNA assay, which overestimated abundance across the full range of concentrations analysed, indicative of a copy number difference between the bloom population and a culture used for assay calibration a priori. In contrast, the sxtA assay performed more consistently, indicating less copy number variation. The sxtA assay was generally reliable, fast and effective in quantifying A. catenella and was predictive of PST contamination of shellfish.
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http://dx.doi.org/10.1038/s41598-019-51074-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787220PMC
October 2019

Pseudo-nitzschia bloom dynamics in the Gulf of Maine: 2012-2016.

Harmful Algae 2019 09 19;88:101656. Epub 2019 Aug 19.

University of Maine, Orono, ME 04469, USA. Electronic address:

The toxic diatom genus Pseudo-nitzschia is a growing presence in the Gulf of Maine (GOM), where regionally unprecedented levels of domoic acid (DA) in 2016 led to the first Amnesic Shellfish Poisoning closures in the region. However, factors driving GOM Pseudo-nitzschia dynamics, DA concentrations, and the 2016 event are unclear. Water samples were collected at the surface and at depth in offshore transects in summer 2012, 2014, and 2015, and fall 2016, and a weekly time series of surface water samples was collected in 2013. Temperature and salinity data were obtained from NERACOOS buoys and measurements during sample collection. Samples were processed for particulate DA (pDA), dissolved nutrients (nitrate, ammonium, silicic acid, and phosphate), and cellular abundance. Species composition was estimated via Automated Ribosomal Intergenic Spacer Analysis (ARISA), a semi-quantitative DNA finger-printing tool. Pseudo-nitzschia biogeography was consistent in the years 2012, 2014, and 2015, with greater Pseudo-nitzschia cell abundance and P. plurisecta dominance in low-salinity inshore samples, and lower Pseudo-nitzschia cell abundance and P. delicatissima and P. seriata dominance in high-salinity offshore samples. During the 2016 event, pDA concentrations were an order of magnitude higher than in previous years, and inshore-offshore contrasts in biogeography were weak, with P. australis present in every sample. Patterns in temporal and spatial variability confirm that pDA increases with the abundance and the cellular DA of Pseudo-nitzschia species, but was not correlated with any one environmental factor. The greater pDA in 2016 was caused by P. australis - the observation of which is unprecedented in the region - and may have been exacerbated by low residual silicic acid. The novel presence of P. australis may be due to local growth conditions, the introduction of a population with an anomalous water mass, or both factors. A definitive cause of the 2016 bloom remains unknown, and continued DA monitoring in the GOM is warranted.
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http://dx.doi.org/10.1016/j.hal.2019.101656DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6779423PMC
September 2019

Development and Validation of PCR-RFLP Assay for Identification of species in the Greater Caribbean region.

J Appl Phycol 2018 Dec 7;30(6):3529-3540. Epub 2018 May 7.

Marine Science Institute - University of Texas at Austin, Port Aransas, USA.

The genus is a recognized group of marine epiphytic-benthic dinoflagellates that produce the toxins that cause ciguatera fish poisoning (CFP). To date, thirteen species and six ribotypes of have been identified, and multiple species commonly co-occur within a single site or epiphyte community. Toxicity can vary by species, thus it is important to be able to differentiate among species for research and monitoring purposes. species have very similar morphological characteristics and are difficult or impossible to distinguish using light microscopy. DNA sequencing has been an important tool in the definition of species, but it can be time-consuming and relatively expensive. To provide an alternative approach, a PCR-RFLP protocol was developed for efficient, rapid, and cost-effective identification of strains isolated from the Gulf of Mexico and Caribbean Sea, where CFP cases and spp. have been reported. The assay targets the D1-D2 hypervariable regions of the large subunit ribosomal RNA gene and uses a single restriction enzyme, BsrI. This method produces distinct RFLP banding patterns for the six species of reported from the Gulf of Mexico and Caribbean Sea, and also distinguishes them from four Pacific endemic species. This method was successfully used to type 465 clonal isolates of from the U.S. Virgin Islands and Akumal Beach - Mexico This BsrI PCR-RFLP method expands the tools available to researchers and managers engaged in monitoring activities and ecological studies.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6759227PMC
December 2018

Spatiotemporal genetic structure of regional-scale Alexandrium catenella dinoflagellate blooms explained by extensive dispersal and environmental selection.

Harmful Algae 2019 06 21;86:46-54. Epub 2019 May 21.

Marine Science Institute, University of Texas at Austin, Port Aransas, TX, 78373, USA. Electronic address:

Paralytic Shellfish Poisoning (PSP) caused by the dinoflagellate Alexandrium catenella is a well-known global syndrome that negatively impacts human health and fishery economies. Understanding the population dynamics and ecology of this species is thus important for identifying determinants of blooms and associated PSP toxicity. Given reports of extensive genetic heterogeneity in the toxicity and physiology of Alexandrium species, knowledge of genetic population structure in harmful algal species such as A. catenella can also facilitate the understanding of toxic bloom development and ecological adaptation. In this study we employed microsatellite markers to analyze multiple A. catenella strains isolated from several sub-regions in the Gulf of Maine (GoM) during summer blooms, to gain insights into the sources and dynamics of this economically important phytoplankton species. At least three genetically distinct clusters of A. catenella were identified in the GoM. Each cluster contained representatives from different sub-regions, highlighting the extent of connectivity and dispersal throughout the region. This shared diversity could result from cyst beds created by previous coastal blooms, thereby preserving the overall diversity of the regional A. catenella population. Rapid spatiotemporal genetic differentiation of A. catenella populations was observed in local blooms, likely driven by natural selection through environmental conditions such as silicate and nitrate/nitrite concentrations, emphasizing the role of short-term water mass intrusions and biotic processes in determining the diversity and dynamics of marine phytoplankton populations. Given the wide-spread intraspecific diversity of A. catenella in GoM and potentially elsewhere, harmful algal blooms will likely persist in many regions despite global warming and changing environmental conditions in the future. Selection of different genetic lineages through variable hydrological conditions might impact toxin production and profiles of future blooms, challenging HAB control and prediction of PSP risk in the future.
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http://dx.doi.org/10.1016/j.hal.2019.03.013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668924PMC
June 2019

Genetic relatedness of a new Japanese isolates of Alexandrium ostenfeldii bloom population with global isolates.

Harmful Algae 2019 04 18;84:64-74. Epub 2019 Mar 18.

National Research Institute of Fisheries Science, Yokohama, Kanagawa, 236-8648, Japan. Electronic address:

In recent years, blooms of toxic Alexandrium ostenfeldii strains have been reported from around the world. In 2013, the species formed a red tide in a shallow lagoon in western Japan, which was the first report of the species in the area. To investigate the genetic relatedness of Japanese A. ostenfeldii and global isolates, the full-length SSU, ITS and LSU sequences were determined, and phylogenetic analyses were conducted for isolates from western and northern Japan and from the Baltic Sea. Genotyping and microsatellite sequence comparison were performed to estimate the divergence and connectivity between the populations from western Japan and the Baltic Sea. In all phylogenetic analyses, the isolates from western Japan grouped together with global isolates from shallow and low saline areas, such as the Baltic Sea, estuaries on the east coast of U.S.A. and from the Bohai Sea, China. In contrast, the isolates from northern Japan formed a well-supported separate group in the ITS and LSU phylogenies, indicating differentiation between the Japanese populations. This was further supported by the notable differentiation between the sequences of western and northern Japanese isolates, whereas the lowest differentiation was found between the western Japanese and Chinese isolates. Microsatellite genotyping revealed low genetic diversity in the western Japanese population, possibly explained by a recent introduction to the lagoon from where it was detected. The red tide recorded in the shallow lagoon followed notable changes in the salinity of the waterbody and phytoplankton composition, potentially facilitating the bloom of A. ostenfeldii.
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http://dx.doi.org/10.1016/j.hal.2019.02.005DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6540814PMC
April 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

Quantitative Response of Alexandrium catenella Cyst Dormancy to Cold Exposure.

Protist 2018 11 18;169(5):645-661. Epub 2018 Jun 18.

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

Many dinoflagellate cysts experience dormancy, a reversible state that prevents germination during unfavorable periods. Several of these species also cause harmful algal blooms (HABs), so a quantitative understanding of dormancy cycling is desired for better prediction and mitigation of bloom impacts. This study examines the effect of cold exposure on the duration of dormancy in Alexandrium catenella, a HAB dinoflagellate that causes paralytic shellfish poisoning (PSP). Mature, dormant cysts from Nauset Marsh (Cape Cod, MA USA) were stored at low but above freezing temperatures for up to six months. Dormancy status was then determined at regular intervals using a germination assay. Dormancy timing was variable among temperatures and was shorter in colder treatments, but the differences collapse when temperature and duration of storage are scaled by chilling-units (CU), a common horticultural predictor of plant and insect development in response to weather. Cysts within Nauset meet a well-defined chilling requirement by late January, after which they are poised to germinate with the onset of favorable conditions in spring. Cysts thus modulate their dormancy cycles in response to their temperature history, enhancing the potential for new blooms and improving this species' adaptability to both unseasonable weather and new habitats/climate regimes.
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http://dx.doi.org/10.1016/j.protis.2018.06.001DOI Listing
November 2018

Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum.

Harmful Algae 2018 07 18;77:43-54. Epub 2018 Jun 18.

Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, United States.

Predator-prey interactions of planktonic protists are fundamental to plankton dynamics and include prey selection, detection, and capture as well as predator detection and avoidance. Propulsive, morphology-specific behaviors modulate these interactions and therefore bloom dynamics. Here, interactions between the mixotrophic, harmful algal bloom (HAB) dinoflagellate Dinophysis acuminata and its ciliate prey Mesodinium rubrum were investigated through quantitative microvideography using a high-speed microscale imaging system (HSMIS). The dinoflagellate D. acuminata is shown to detect its M. rubrum prey via chemoreception while M. rubrum is alerted to D. acuminata via mechanoreception at much shorter distances (89 ± 39 μm versus 41 ± 32 μm). On detection, D. acuminata approaches M. rubrum with reduced speed. The ciliate M. rubrum responds through escape jumps that are long enough to detach its chemical trail from its surface, thereby disorienting the predator. To prevail, D. acuminata uses capture filaments and/or releases mucus to slow and eventually immobilize M. rubrum cells for easier capture. Mechanistically, results support the notion that the desmokont flagellar arrangement of D. acuminata lends itself to phagotrophy. In particular, the longitudinal flagellum plays a dominant role in generating thrust for the cell to swim forward, while at other times, it beats to supply a tethering or anchoring force to aid the generation of a posteriorly-directed, cone-shaped scanning current by the transverse flagellum. The latter is strategically positioned to generate flow for enhanced chemoreception and hydrodynamic camouflage, such that D. acuminata can detect and stealthily approach resting M. rubrum cells in the water column.
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http://dx.doi.org/10.1016/j.hal.2018.06.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6089243PMC
July 2018

Microbial Community Structure and Associations During a Marine Dinoflagellate Bloom.

Front Microbiol 2018 6;9:1201. Epub 2018 Jun 6.

Shenzhen Public Platform for Screening and Application of Marine Microbial Resources, Graduate School at Shenzhen, Tsinghua University, Shenzhen, China.

Interactions between microorganisms and algae during bloom events significantly impacts their physiology, alters ambient chemistry, and shapes ecosystem diversity. The potential role these interactions have in bloom development and decline are also of particular interest given the ecosystem impacts of algal blooms. We hypothesized that microbial community structure and succession is linked to specific bloom stages, and reflects complex interactions among taxa comprising the phycosphere environment. This investigation used pyrosequencing and correlation approaches to assess patterns and associations among bacteria, archaea, and microeukaryotes during a spring bloom of the dinoflagellate . Within the bacterial community, and were predominant during the initial bloom stage, while , and were the most abundant taxa present during bloom onset and termination. In the archaea biosphere, methanogenic members were present during the early bloom period while the majority of species identified in the late bloom stage were ammonia-oxidizing archaea and . Dinoflagellates were the major eukaryotic group present during most stages of the bloom, whereas a mixed assemblage comprising diatoms, green-algae, rotifera, and other microzooplankton were present during bloom termination. Temperature and salinity were key environmental factors associated with changes in bacterial and archaeal community structure, respectively, whereas inorganic nitrogen and inorganic phosphate were associated with eukaryotic variation. The relative contribution of environmental parameters measured during the bloom to variability among samples was 35.3%. Interaction analysis showed that Maxillopoda, Spirotrichea, Dinoflagellata, and were keystone taxa within the positive-correlation network, while , Dictyochophyceae, Mamiellophyceae, and were the main contributors to the negative-correlation network. The positive and negative relationships were the primary drivers of mutualist and competitive interactions that impacted algal bloom fate, respectively. Functional predictions showed that blooms enhance microbial carbohydrate and energy metabolism, and alter the sulfur cycle. Our results suggest that microbial community structure is strongly linked to bloom progression, although specific drivers of community interactions and responses are not well understood. The importance of considering biotic interactions (e.g., competition, symbiosis, and predation) when investigating the link between microbial ecological behavior and an algal bloom's trajectory is also highlighted.
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http://dx.doi.org/10.3389/fmicb.2018.01201DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5998739PMC
June 2018

Estrogenic potency of MC-LR is induced via stimulating steroidogenesis: In vitro and in vivo evidence.

Environ Pollut 2018 Sep 14;240:615-622. Epub 2018 May 14.

College of Fisheries, Huazhong Agricultural University, Wuhan 430070, PR China; Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Wuhan 430070, PR China; Hubei Provincial Engineering Laboratory for Pond Aquaculture, Wuhan 430070, PR China; National Demonstration Center for Experimental Aquaculture Education (Huazhong Agricultural University), Wuhan 430070, PR China.

Waterborne microcystin-LR (MC-LR) has been reported to disrupt sex hormones, while its estrogenic potency remains controversial. We hypothesized that MC-LR could induce estrogenic effects via disrupting sex hormone synthesis, and verified this hypothesis by in vitro and in vivo assays. Effects of MC-LR (1, 10, 100, 500, 1000 and 5000 μg/L) on steroidogenesis were assessed in the H295R cells after 48 h. The contents of 17β-estradiol (E2) and testosterone (T) increased in a non-dose-dependent manner, which showed positive correlations with the expression of steroidogenic genes. In the in vivo assay, adult male zebrafish were exposed to 0.3, 1, 3, 10 and 30 μg/L MC-LR for 30 d. Similarly, E2 and T contents in the testis were increased, accompanied by extensive up-regulation of steroidogenic genes, especially cyp19a. Meanwhile, the percentage of spermatid in the testis declined. In the liver, the vtg1 gene was significantly up-regulated while both the transcriptional and protein levels of the estrogenic receptor (ER) declined. These results indicate that MC-LR induced non-dose-dependent estrogenic effects at environmental concentrations, which may result from steroidogenesis stimulation via a non-ER-mediated pathway. Our findings support a paradigm shift in the risk assessment of MC-LR from traditional toxicity to estrogenic risk, particularly at low concentrations, and emphasize the potential threat to the male reproductive capacity of wildlife in bloom areas.
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http://dx.doi.org/10.1016/j.envpol.2018.04.140DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6859840PMC
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

Bloom termination of the toxic dinoflagellate : Vertical migration behavior, sediment infiltration, and benthic cyst yield.

Limnol Oceanogr 2017 11 5;62(6):2829-2849. Epub 2017 Oct 5.

Biology Department Woods Hole Oceanographic Institution Woods Hole Massachusetts.

New resting cyst production is crucial for the survival of many microbial eukaryotes including phytoplankton that cause harmful algal blooms. Production in situ has previously been estimated through sediment trap deployments, but here was instead assessed through estimation of the total number of planktonic cells and new resting cysts produced by a localized, inshore bloom of , a dinoflagellate that is a globally important cause of paralytic shellfish poisoning. Our approach utilizes high frequency, automated water monitoring, weekly observation of new cyst production, and pre- and post-bloom spatial surveys of total resting cyst abundance. Through this approach, new cyst recruitment within the study area was shown to account for at least 10.9% ± 2.6% (SE) of the bloom's decline, ∼ 5× greater than reported from comparable, sediment trap based studies. The observed distribution and timing of new cyst recruitment indicate that: (1) planozygotes, the immediate precursor to cysts in the life cycle, migrate nearer to the water surface than other planktonic stages and (2) encystment occurs after planozygote settlement on bottom sediments. Near surface localization by planozygotes explains the ephemerality of red surface water discoloration by blooms, and also enhances the dispersal of new cysts. Following settlement, bioturbation and perhaps active swimming promote sediment infiltration by planozygotes, reducing the extent of cyst redistribution between blooms. The concerted nature of bloom sexual induction, especially in the context of an observed upper limit to bloom intensities and heightened susceptibility of planozygotes to the parasite , is also discussed.
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http://dx.doi.org/10.1002/lno.10664DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5725721PMC
November 2017

Assessing the use of artificial substrates to monitor Gambierdiscus populations in the Florida Keys.

Harmful Algae 2017 09 29;68:52-66. Epub 2017 Jul 29.

Biology Department, MS #32, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.

Four distinct coastal locations were sampled on a monthly basis near Long Key (Florida Keys, USA) over a 13-month period to study Gambierdiscus population dynamics on different substrates, including four macrophyte species (Dictyota spp., Halimeda spp., Laurencia spp., and Thalassia testudinum) and three artificial substrates (polyvinyl chloride (PVC) tiles, burlap, and fiberglass window screen). Cell densities of Gambierdiscus were generally lower on Dictyota versus Halimeda and Laurencia. Cell densities of Gambierdiscus were significantly correlated among macrophyte hosts in 54% of the comparisons, and between macrophyte hosts and artificial substrates in 72% of the comparisons. Predictive slopes determined from regression analyses between cell densities on artificial substrates and macrophyte hosts indicated that, on an areal basis, fewer cells were present on macrophytes versus artificial substrates (cells cm) and that slope variation (error) among the different macrophytes and sites ranged from 5% to 200%, averaging 61% overall. As the data required log-transformation prior to analyses, this level of error translates into two-orders of magnitude in range of estimation of the overall average abundance of Gambierdiscus cells on macrophytes (135 cells g wet weight); 20-2690 cells g ww. The lack of consistent correlation among Gambierdiscus cell densities on macrophytes versus artificial substrates, coupled with the high level of error associated with the predictive slope estimations, indicates that extreme caution should be taken when interpreting the data garnered from artificial substrate deployments, and that such deployments should be thoroughly vetted prior to routine use for monitoring purposes.
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http://dx.doi.org/10.1016/j.hal.2017.07.007DOI Listing
September 2017

The prevalence of benthic dinoflagellates associated with ciguatera fish poisoning in the central Red Sea.

Harmful Algae 2017 09 9;68:206-216. Epub 2017 Sep 9.

Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, Jeddah, 23955, Kingdom of Saudi Arabia.

This study confirms the presence of the toxigenic benthic dinoflagellates Gambierdiscus belizeanus and Ostreopsis spp. in the central Red Sea. To our knowledge, this is also the first report of these taxa in coastal waters of Saudi Arabia, indicating the potential occurrence of ciguatera fish poisoning (CFP) in that region. During field investigations carried out in 2012 and 2013, a total of 100 Turbinaria and Halimeda macroalgae samples were collected from coral reefs off the Saudi Arabian coast and examined for the presence of Gambierdiscus and Ostreopsis, two toxigenic dinoflagellate genera commonly observed in coral reef communities around the world. Both Gambierdiscus and Ostreopsis spp. were observed at low densities (<200 cells g wet weight algae). Cell densities of Ostreopsis spp. were significantly higher than Gambierdiscus spp. at most of the sampling sites, and abundances of both genera were negatively correlated with seawater salinity. To assess the potential for ciguatoxicity in this region, several Gambierdiscus isolates were established in culture and examined for species identity and toxicity. All isolates were morphologically and molecularly identified as Gambierdiscus belizeanus. Toxicity analysis of two isolates using the mouse neuroblastoma cell-based assay for ciguatoxins (CTX) confirmed G. belizeanus as a CTX producer, with a maximum toxin content of 6.50±1.14×10pg P-CTX-1 eq. cell. Compared to Gambierdiscus isolates from other locations, these were low toxicity strains. The low Gambierdiscus densities observed along with their comparatively low toxin contents may explain why CFP is unidentified and unreported in this region. Nevertheless, the presence of these potentially toxigenic dinoflagellate species at multiple sites in the central Red Sea warrants future study on their possible effects on marine food webs and human health in this region.
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http://dx.doi.org/10.1016/j.hal.2017.08.005DOI Listing
September 2017

Differential cellular responses associated with oxidative stress and cell fate decision under nitrate and phosphate limitations in Thalassiosira pseudonana: Comparative proteomics.

PLoS One 2017 14;12(9):e0184849. Epub 2017 Sep 14.

School of Life Sciences, Xiamen University, Xiamen, China.

Diatoms are important components of marine ecosystems and contribute greatly to the world's primary production. Despite their important roles in ecosystems, the molecular basis of how diatoms cope with oxidative stress caused by nutrient fluctuations remains largely unknown. Here, an isobaric tags for relative and absolute quantitation (iTRAQ) proteomic method was coupled with a series of physiological and biochemical techniques to explore oxidative stress- and cell fate decision-related cellular and metabolic responses of the diatom Thalassiosira pseudonana to nitrate (N) and inorganic phosphate (P) stresses. A total of 1151 proteins were detected; 122 and 56 were significantly differentially expressed from control under N- and P-limited conditions, respectively. In N-limited cells, responsive proteins were related to reactive oxygen species (ROS) accumulation, oxidative stress responses and cell death, corresponding to a significant decrease in photosynthetic efficiency, marked intracellular ROS accumulation, and caspase-mediated programmed cell death activation. None of these responses were identified in P-limited cells; however, a significant up-regulation of alkaline phosphatase proteins was observed, which could be the major contributor for P-limited cells to cope with ambient P deficiency. These findings demonstrate that fundamentally different metabolic responses and cellular regulations are employed by the diatom in response to different nutrient stresses and to keep the cells viable.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0184849PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5599023PMC
October 2017

Effects of an allelochemical in Phaeodactylum tricornutum filtrate on Heterosigma akashiwo: Morphological, physiological and growth effects.

Chemosphere 2017 Nov 7;186:527-534. Epub 2017 Aug 7.

Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, United States.

The effects of an allelochemical extracted from the culture filtrate of diatom Phaeodactylum tricornutum on the raphidophyte Heterosigma akashiwo were investigated using a series of morphological, physiological and biochemical characters. Growth experiments showed that H. akashiwo was significantly inhibited immediately after exposure to the allelochemical, with many cells rapidly dying and lysing based on microscopic observation. The effects of the allelochemical on the surviving cells were explored using Scanning Electron Microscopy (SEM) and Flow cytometry (FCM), the latter by examination of a suite of physiological parameters (membrane integrity, esterase activity, chlorophyll-a content, membrane potential). The results demonstrate that the membrane of H. akashiwo was attacked by the allelochemical directly, causing cell membrane breakage and loss of integrity. Esterase activity was the most sensitive indicator of the impacts of the allelochemical. Membrane potential and chlorophyll-a content both showed significant decreases following exposure of the Heterosigma cells to high concentrations of the allelochemical for 5 and 6 days. Both were affected, but the membrane potential response was more gradual compared to other effects. The cell size of H. akashiwo did not change compared with the control group. The surviving cells were able to continue to grow and in a few days, re-establish a successful culture, even in the presence of residual allelochemical, suggesting either development of cellular resistance, or the degradation of the chemical.
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http://dx.doi.org/10.1016/j.chemosphere.2017.08.024DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6507415PMC
November 2017

Insights into the loss factors of phytoplankton blooms: The role of cell mortality in the decline of two inshore blooms.

Limnol Oceanogr 2017 Jul 23;62(4):1742-1753. Epub 2017 Mar 23.

The University of Texas at Austin, Marine Science Institute, Port Aransas, TX 78373 USA.

While considerable effort has been devoted to understanding the factors regulating the development of phytoplankton blooms, the mechanisms leading to bloom decline and termination have received less attention. Grazing and sedimentation have been invoked as the main routes for the loss of phytoplankton biomass, and more recently, viral lysis, parasitism and programmed cell death (PCD) have been recognized as additional removal factors. Despite the importance of bloom declines to phytoplankton dynamics, the incidence and significance of various loss factors in regulating phytoplankton populations have not been widely characterized in natural blooms. To understand mechanisms controlling bloom decline, we studied two independent, inshore blooms of , paying special attention to cell mortality as a loss pathway. We observed increases in the number of dead cells with PCD features after the peak of both blooms, demonstrating a role for cell mortality in their terminations. In both blooms, sexual cyst formation appears to have been the dominant process leading to bloom termination, as both blooms were dominated by small-sized gamete cells near their peaks. Cell death and parasitism became more significant as sources of cell loss several days after the onset of bloom decline. Our findings show two distinct phases of bloom decline, characterized by sexual fusion as the initial dominant cell removal processes followed by elimination of remaining cells by cell death and parasitism.
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http://dx.doi.org/10.1002/lno.10530DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6426133PMC
July 2017
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