Marine Algal Blooms Research Articles

Dynamic patterns of carbohydrate metabolism genes in bacterioplankton during marine algal blooms

Carbohydrates play a pivotal role in nutrient recycling and regulation of algal–bacterial interactions. Despite their ecological significance, the intricate molecular mechanisms governing regulation of phycosphere carbohydrates by bacterial taxa linked with natural algal bloom have yet to be fully elucidated. Here, a comprehensive temporal metagenomic analysis was conducted to explore the carbohydrate-active enzyme (CAZyme) genes in two discrete algal bloom microorganisms (Gymnodinium catenatum and Phaeocystis globosa) across three distinct bloom stages: pre-bloom, peak bloom, and post-bloom. Elevated levels of extracellular carbohydrates, primarily rhamnose, galactose, glucose, and arabinose, were observed during the initial and post-peak stages. The prominent CAZyme families identified—glycoside hydrolases (GH) and carbohydrate-binding modules (CBMs)—were present in both algal bloom occurrences. In the G. catenatum bloom, GH23/24 and CBM13/14 were prevalent during the pre-bloom and peak bloom stages, whereas GH2/3/30 and CBM12/24 exhibited increased prevalence during the post-bloom phase. In contrast, the P. globosa bloom had a dominance of GH13/23 and CBM19 in the initial phase, and this was succeeded by GH3/19/24/30 and CBM54 in the later stages. This gene pool variation—observed distinctly in specific genera—highlighted the dynamic structural shifts in functional resources driven by temporal alterations in available substrates. Additionally, ecological linkage analysis underscored a correlation between carbohydrates (or their related genes) and phycospheric bacteria, hinting at a pattern of bottom-up control. These findings contribute to understanding of the dynamic nature of CAZymes, emphasizing the substantial influence of substrate availability on the metabolic capabilities of algal symbiotic bacteria, especially in terms of carbohydrates.

Analysis of long-term changes in algal bloom pattern and their association with Ocean, atmosphere, and land-based processes across the northern Indian Ocean

Algal blooms are global phenomena in marine and fresh waters. An understanding of the impacts of climate change and anthropogenic activities on marine algal blooms is essential for protecting marine ecosystems. We have studied the long-term changes in the spatial patterns of algal blooms over the northern Indian Ocean and assessed the influence of the ocean, atmosphere, and land-based processes on them. We have analyzed multi-source satellite data (2003 – 2020) of various parameters such as algal concentration, temperature, salinity, sea level, particulate organic carbon, precipitation, wind speed, and river discharge on an open-source cloud computing platform. The seasonality of variables is assessed using a harmonic model, and their spatial trend is estimated using the non-parametric Mann-Kendall test. The spatial relationship between various geophysical parameters and algal bloom concentration is assessed by the cross-correlation test, and the prediction is done using a multivariate autoregression model. Results suggest that each variable exhibits distinguishable seasonal patterns. Algal bloom duration showed a significant increase over time. However, algal bloom coverage showed a significant decline in the coastal waters in all seasons except post-monsoon. The cross-correlation test unveils that lower temperatures, salinity, and sea level promote algal bloom occurrences in coastal waters rather than open waters. Furthermore, the statistical model with a time lag of 2 months shows better performance for prediction of bloom intensity (r2 = 0.86).

A rapid assessment method to monitor the health status of habitat‐forming species in coastal benthic ecosystems

Abstract Marine habitat‐forming (MHF) species in the Mediterranean are among the most threatened coastal species by human activities. In recent decades, different stressors (e.g., warming‐induced marine heatwaves and algal blooms) have caused mass mortality events in these key species. Overall, a common method to assess their health status at the Mediterranean Sea scale is lacking. To fill this gap, the aim of this work is to present and validate a cost‐effective method, the Mortality Rapid Assessment Method, that is able to assess the health status of key MHF species, even through Citizen Science. The Mortality Rapid Assessment Method is based on determining the impact of mortality on MHF species derived from the metric percentage of affected colonies or individuals. To validate the ability of the proposed method to assess the health status, it was compared to a more commonly used but time‐consuming and expert‐required metric based on the injured surface percentage of the colonies or individuals. For the validation, one of the most extensive (>47,500 colonies) demographic datasets of the octocoral Paramuricea clavata was used to conduct a comprehensive metric comparison. The results showed a highly significant correlation between metrics from both methods (ρ = 0.86), confirming that the percentage of affected colonies provides a reliable assessment of the health status of gorgonian populations over broad spatial and temporal scales. Bearing in mind that this metric can be applied to different MHF species, such as sponges, bryozoans and calcareous algae, and by non‐scientific personnel (managers and trained volunteers), its implementation can contribute to inform and enhance the effectiveness of the conservation and management plans for key MHF species at the scale of the Mediterranean Sea.

Chattonella marina blooms in a trophic gradient system: Interaction with environmental drivers

For coastal eutrophication, lots of studies focused on the influence from environmental factors, especially nitrogen and phosphorus, on algae blooms. The interaction between algae and environmental factors has been often ignored. Using Chattonella marina, a dominant species in marine algal blooms, we established a trophic gradient system that simulated C. marina blooms at three trophic levels: eutrophic, mesotrophic, and oligotrophic, and examined the life history patterns of C. marina and the interactions with environmental factors. Increased trophic levels influenced the growth potential of C. marina, while its unique cyst reproduction allowed it to thrive in nutrient-limited environments. Adequate nutrients caused changes in dissolved oxygen (DO) and pH led by C. marina, with the carbonate system playing a crucial role in regulating pH under nutrient-limited conditions. Limiting the growth of C. marina in areas with low nutrient by manipulating reactive silicate (SiO32−) availability may prove effective. Nitrate (NO3−) was the preferred nutrient for C. marina when its concentration exceeded that of ammonium (NH4+). Phosphorus played a crucial role in the growth and proliferation of C. marina, especially when other nutrients were scarce. The findings of this study may provide valuable insights into the effective management and prevention of algae blooms.

Role of marine algal blooms in the release of arsenic at the sediment-seawater interface: Evidence from microcosm experiments

Algal blooms can aggravate arsenic (As) release from sediments and thus pose a pollution risk in the marine environment. However, the driving mechanism of algal blooms on sedimentary As cycling remains unclear. This study undertakes the first comprehensive examination of As release mechanisms under algal bloom conditions based on the evidence provided by temporal and depth profile changes of As species in the overlying water column, porewater and sediment, as well as As-related functional genes over the course of a 30-day incubation experiment using algal addition. The higher rate of increase of dissolved total As (dTAs) concentrations in a high biomass algal group (HAG) than an experimental control group (CG) suggested that algal degradation promoted the release of sedimentary As. The solid phase in all experimental groups remained rich in As(V), while in porewater As(III) and As(V) were the dominant As species during the initial rapid and subsequent slow degradation phases of organic matter, respectively, indicating that microbial reduction of As(V) and Fe(III) controlled the release of As during these two periods. A pronounced increase in arrA gene copies, and not a corresponding increase in the Geobacter copies, in HAG relative to CG supported the notion that algal blooms promoted microbial As(V) reduction. Additionally, the lower concentration of dissolved As(III) and cumulative dTAs flux in the sterilized-HAG treatment than in the sterilized-CG one further suggested that geochemically-mediated processes were not the main pathways of As release. Finally, it is estimated that summer algal blooms in the Changjiang Estuary can cause the release of 1440 kg of sedimentary As into the overlying water.

Coastal phytoplankton blooms expand and intensify in the 21st century

Phytoplankton blooms in coastal oceans can be beneficial to coastal fisheries production and ecosystem function, but can also cause major environmental problems1,2—yet detailed characterizations of bloom incidence and distribution are not available worldwide. Here we map daily marine coastal algal blooms between 2003 and 2020 using global satellite observations at 1-km spatial resolution. We found that algal blooms occurred in 126 out of the 153 coastal countries examined. Globally, the spatial extent (+13.2%) and frequency (+59.2%) of blooms increased significantly (P < 0.05) over the study period, whereas blooms weakened in tropical and subtropical areas of the Northern Hemisphere. We documented the relationship between the bloom trends and ocean circulation, and identified the stimulatory effects of recent increases in sea surface temperature. Our compilation of daily mapped coastal phytoplankton blooms provides the basis for global assessments of bloom risks and benefits, and for the formulation or evaluation of management or policy actions.

Integrative monitoring strategy for marine and freshwater harmful algal blooms and toxins across the freshwater-to-marine continuum.

Many coastal states throughout the USA have observed negative effects in marine and estuarine environments caused by cyanotoxins produced in inland waterbodies that were transported downstream or produced in the estuaries. Estuaries and other downstream receiving waters now face the dual risk of impacts from harmful algal blooms (HABs) that occur in the coastal ocean as well as those originating in inland watersheds. Despite this risk, most HAB monitoring efforts do not account for hydrological connections in their monitoring strategies and designs. Monitoring efforts in California have revealed the persistent detection of cyanotoxins across the freshwater-to-marine continuum. These studies underscore the importance of inland waters as conduits for the transfer of cyanotoxins to the marine environment and highlight the importance of approaches that can monitor across hydrologically connected waterbodies. A HAB monitoring strategy is presented for the freshwater-to-marine continuum to inform HAB management and mitigation efforts and address the physical and hydrologic challenges encountered when monitoring in these systems. Three main recommendations are presented based on published studies, new datasets, and existing monitoring programs. First, HAB monitoring would benefit from coordinated and cohesive efforts across hydrologically interconnected waterbodies and across organizational and political boundaries and jurisdictions. Second, a combination of sampling modalities would provide the most effective monitoring for HAB toxin dynamics and transport across hydrologically connected waterbodies, from headwater sources to downstream receiving waterbodies. Third, routine monitoring is needed for toxin mixtures at the land-sea interface including algal toxins of marine origins as well as cyanotoxins that are sourced from inland freshwater or produced in estuaries. Case studies from California are presented to illustrate the implementation of these recommendations, but these recommendations can also be applied to inland states or regions where the downstream receiving waterbody is a freshwater lake, reservoir, or river. Integr Environ Assess Manag 2023;19:586-604. © 2022 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).

Motile microorganisms in complex fluids

The interaction of motile microorganisms and surrounding fluids is of importance in a variety of biological and environmental phenomena including the development of biofilms, colonization of microbes in human and animal bodies, and formation of marine algal blooms. Complex fluids are pervasive in microbial environments and can have profound effects on the motility of microbes, affecting fundamental microbial processes such as their ability to take up nutrients and colonize surfaces. In this study, we scrutinize the role of rheological properties of the surrounding fluid on the motility, spatial distribution, and collective behaviour of microswimmers in complex fluids.

Dynamic patterns of quorum sensing signals in phycospheric microbes during a marine algal bloom

In the marine environment, the interactions among various species based on chemical signals play critical roles in influencing microbial structure and function. Quorum sensing (QS), the well-known signal-dependent communication autoinducer, is an important regulator in complex microbial communities. Here, we explored the QS gene profiles of phycosphere bacteria during a microcosmic phytoplankton bloom using metagenomic sequence data. More than fifteen subtypes of QS systems and 211,980 non-redundant amino acid sequences were collected and classified for constructing a hierarchical quorum-sensing database. The abundance of the various QS subtypes varied at different bloom stages and showed a strong correlation with phycosphere microorganisms. This suggested that QS is involved in regulating the phycosphere microbial succession during an algal bloom. A neutral community model revealed that the QS functional gene community assemblies were driven by stochastic processes. Co-occurrence model analysis showed that the QS gene networks of phycospheric microbes had similar topological structure and functional composition, which is a potential cornerstone for maintaining signal communication and population stabilization among microorganisms. Overall, QS systems have a strong relationship with the development of algal blooms and participate in regulating algal-associated microbial communities as chemical signals. This research reveals the chemical and ecological behavior of algal symbiotic bacteria and expands the current understanding of microbial dynamics in marine algal blooms.

Sub-lethal and lethal effects of chronic and extreme multiple stressors on a critical New Zealand bivalve under hypoxia

Warming of coastal regions due to climate change is exerting chronic thermal stress on intertidal organisms, many of which are already living at or near their limits for thermal tolerance. In addition, increasing frequency of marine heat waves and algal blooms leading to hypoxic events in estuaries exert acute stresses on aerobic organisms. Hypoxia and warming rarely occur in isolation, and when combined, likely have synergistic detrimental effects on bivalves. Further, midday low tides have been identified as important drivers of mass mortality events for bivalves as a consequence of the combined effects of thermal stress and desiccation. Accordingly, the current study focuses on the sublethal and lethal effects of these combined stressors on the critical estuarine bivalve Austrovenus stutchburyi. Experiments were used to test the effects of simulated midday low tides combined with chronic warming and oxygen depletion on activity, respiration and survival of A. stutchburyi. A lethal emersion thermal threshold was surpassed at 33°C for treatments exposed to both hypoxic and normoxic treatments, suggesting extreme thermal events such as heatwaves during midday low tides could have substantial detrimental effects on bivalve populations and their vital ecosystem functions. Further, the ability of bivalves to survive heat and desiccation of midday low tide events was much reduced when they were exposed to even minor heat and hypoxia stress when immersed at high tide. The findings of the current study highlight important biological consequences of coastal warming combined with extreme temperature and hypoxic events observed in estuaries.

Toxin Analysis of Freshwater Cyanobacterial and Marine Harmful Algal Blooms on the West Coast of Florida and Implications for Estuarine Environments

Recent marine and freshwater algal and cyanobacterial blooms in Florida have increased public concern and awareness of the risks posed by exposure to these organisms. In 2018, Lake Okeechobee and the Caloosahatchee river, on the west coast of Florida, experienced an extended bloom of Microcystis spp. and a bloom of Karenia brevis in the coastal waters of the Gulf of Mexico that coincided in the Fort Myers area. Samples from the Caloosahatchee at Fort Myers into Pine Island Sound and up to Boca Grande were collected by boat. High concentrations of microcystin-LR were detected in the cyanobacterial bloom along with brevetoxins in the marine samples. Furthermore, β-N-methylamino-L-alanine (BMAA) and isomers N-(2-aminoethyl)glycine (AEG) and 2,4-diaminobuytric acid (DAB) were detected in marine diatoms and dinoflagellates, and cyanobacteria of freshwater origin. High freshwater flows pushed the cyanobacterial bloom to barrier island beaches and Microcystis and microcystins could be detected into the marine environment at a salinity of 41 mS/cm. For comparison, in 2019 collections of Dapis (a new generic segregate from Lyngbya) mats from Sarasota showed high concentrations of BMAA, suggesting the possibility of long-term exposure of residents to BMAA. The findings highlight the potential for multiple, potentially toxic blooms to co-exist and the possible implications for human and animal health.

Polysaccharide niche partitioning of distinct Polaribacter clades during North Sea spring algal blooms

Massive releases of organic substrates during marine algal blooms trigger growth of many clades of heterotrophic bacteria. Algal polysaccharides represent the most diverse and structurally complex class of these substrates, yet their role in shaping the microbial community composition is poorly understood. We investigated, whether polysaccharide utilization capabilities contribute to niche differentiation of Polaribacter spp. (class Flavobacteriia; known to include relevant polysaccharide-degraders) that were abundant during 2009–2012 spring algal blooms in the southern North Sea. We identified six distinct Polaribacter clades using phylogenetic and phylogenomic analyses, quantified their abundances via fluorescence in situ hybridization, compared metagenome-assembled genomes, and assessed in situ gene expression using metaproteomics. Four clades with distinct polysaccharide niches were dominating. Polaribacter 2-a comprised typical first responders featuring small genomes with limited polysaccharide utilization capacities. Polaribacter 3-a were abundant only in 2010 and possessed a distinct sulfated α-glucoronomannan degradation potential. Polaribacter 3-b responded late in blooms and had the capacity to utilize sulfated xylan. Polaribacter 1-a featured high numbers of glycan degradation genes and were particularly abundant following Chattonella algae blooms. These results support the hypothesis that sympatric Polaribacter clades occupy distinct glycan niches during North Sea spring algal blooms.

Biofouling in capillary and spiral wound membranes facilitated by marine algal bloom

Algal-derived organic matter (AOM), particularly transparent exopolymer particles, has been suspected to facilitate biofilm development in membrane systems (e.g., seawater reverse osmosis). This study demonstrates the possible role of AOM on biofouling in membrane systems affected by marine algal blooms. The tendency of AOM from bloom-forming marine algae to adhere to membranes and its ability to enhance biofilm growth were measured using atomic force microscopy, flow cytometry, liquid chromatography and accelerated membrane biofouling experiments. Adhesion force measurements indicate that AOM tends to adhere to clean membranes and even more strongly to AOM-fouled membranes. Batch growth tests illustrate that the capacity of seawater to support bacterial growth can significantly increase with AOM concentration. Biofouling experiments with spiral wound and capillary membranes illustrate that when nutrients availability are not limited in the feed water, a high concentration of AOM – whether in suspension or attached to the membrane – can substantially accelerates biofouling. A significantly lower biofouling rate was observed on membranes exposed to feed water spiked only with AOM or easily biodegradable nutrients. The abovementioned findings indicate that AOM facilitates the onset of membrane biofouling primarily as a conditioning platform and to some extent as a nutrient source for biofilm-forming bacteria.

Effect of physical and chemical stress on ultrafiltration membrane performance during marine algal blooms

ABSTRACTThis study assessed the effects of physical and chemical stresses on marine algae cells Tetraselmis suecica and its implications on ultrafiltration (UF) performance. It was found that physical stress did not have significant effect on membrane fouling performance. Chemical stress by chlorination significantly lysed algae cells and reduced membrane fouling. Physical and chemical stresses increased the low molecular weight organics fractions which have no obvious effect on UF membrane fouling due to its low membrane rejection. However, this reduced the reverse osmosis feed quality significantly. Results indicate the importance of appropriate management of physical and chemical stress parameters in desalination plants.

Development of a quantitative PCR method to explore the historical occurrence of a nuisance microalga under expansion

A number of marine and freshwater harmful algal bloom (HAB) species have colonized new areas and expanded their habitat range in recent years. Nevertheless it is notoriously difficult to establish when colonization first occurred, what the dispersal routes are, and to separate recent invasion from increases in existent but small populations. The freshwater raphidophyte Gonyostomum semen is a nuisance species that has expanded its habitat range and increased in abundance in northern Europe during the past decades. To evaluate to what extent sediments can be used for determining historic occurrence of G. semen, a quantitative real-time PCR method for detecting cysts of this algae was developed. This paper presents a qPCR protocol with a set of primers that are specific to Gonyostomum and with PCR conditions optimized for sediment samples from humic lakes, which are the common habitat of G. semen. With this sensitive method as few as 1.6 cysts per PCR reaction could be reliably quantified, corresponding to 320 cysts per g wet weight sediment. Cysts were present in sediments with ages ranging from years to decades and their persistence allows detection of historic populations up to at least 50 years old. With this qPCR assay it will be possible to trace the presence of G. semen in environments prior to the onset of algae-specific monitoring programs as well as for quantification in water column samples.

Identification of fouling materials in the microfiltration of seawater laden with marine algae

AbstractIn this study, fouling materials were identified in the microfiltration (MF) of seawater laden with marine algae. To this end, raw seawater spiked with either the dinoflagellate species without cell walls (Heterosigma akashiwo) or with cell walls (Prorocentrum micans) was filtered through a laboratory-scale MF system. Based on the results, polysaccharides, which were excreted by the marine algae, accumulated within the MF system and subsequently resulted in membrane fouling. Cell walls are closely related with polysaccharide excretion. The dinoflagellate species without cell walls released more polysaccharides than those with cell walls based on the unit surface area of the species. High-performance size exclusion chromatography analysis revealed that organic substances (1.1 and 22 kDa, molecular weight) were accumulated in the MF system. These organic substances could be the biofouling agents in MF systems during marine algal blooms.

Integrative Monitoring of Marine and Freshwater Harmful Algae in Washington State for Public Health Protection

The more frequent occurrence of both marine and freshwater toxic algal blooms and recent problems with new toxic events have increased the risk for illness and negatively impacted sustainable public access to safe shellfish and recreational waters in Washington State. Marine toxins that affect safe shellfish harvest in the state are the saxitoxins that cause paralytic shellfish poisoning (PSP), domoic acid that causes amnesic shellfish poisoning (ASP) and the first ever US closure in 2011 due to diarrhetic shellfish toxins that cause diarrhetic shellfish poisoning (DSP). Likewise, the freshwater toxins microcystins, anatoxin-a, cylindrospermopsins, and saxitoxins have been measured in state lakes, although cylindrospermopsins have not yet been measured above state regulatory guidance levels. This increased incidence of harmful algal blooms (HABs) has necessitated the partnering of state regulatory programs with citizen and user-fee sponsored monitoring efforts such as SoundToxins, the Olympic Region Harmful Algal Bloom (ORHAB) partnership and the state’s freshwater harmful algal bloom passive (opportunistic) surveillance program that allow citizens to share their observations with scientists. Through such integrated programs that provide an effective interface between formalized state and federal programs and observations by the general public, county staff and trained citizen volunteers, the best possible early warning systems can be instituted for surveillance of known HABs, as well as for the reporting and diagnosis of unusual events that may impact the future health of oceans, lakes, wildlife, and humans.

The great iron dump

The discovery that marine algal blooms deposit organic carbon to the deep ocean answers some — but not all — of the questions about whether fertilizing such blooms is a viable strategy for mitigating climate change. See Article p.313 The iron hypothesis proposes that the supply of iron-bearing dust to certain oceanic regions stimulates phytoplankton blooms that, by sinking out to the deep ocean when the organisms die, sequester carbon absorbed from exchange with the atmosphere. Experiments carried out to test the idea have provided clear evidence that iron addition generates phytoplankton blooms in waters with high -nutrient but low -chlorophyll concentrations, as proposed. But the fate of phytoplankton blooms and hence the extent of any carbon sequestration to the deep ocean has remained uncertain. This paper presents multiple lines of evidence, collected by aboard RV Polarstern in 2004 during the European Iron Fertilization Experiment (EIFEX), that suggest carbon is exported to the deep ocean as a result of iron fertilization, with at least half of the bloom biomass sinking to below 1,000 metres.

Evaluation of Okadaic Acid-Induced Genotoxicity in Human Cells Using the Micronucleus Test and γH2AX Analysis

Marine algal blooms have become a public health concern due to increasing frequency in the environment and severity of exposure consequences. Human intoxications produced by phycotoxins occur globally through consumption of marine fish products containing bioaccumulated toxins. Okadaic acid (OA) is the main representative of diarrheic shellfish poisoning (DSP) toxin. OA was found to inhibit protein phosphatases and to produce oxidative damage, as well as to disturb different cellular functions including cell cycle, gene expression, and DNA repair mechanisms. The aim of this study was to determine whether OA induced genotoxicity by using a micronucleus (MN) test and γH2AX analysis, and to elucidate the underlying mechanisms. Human peripheral blood leukocytes, neuroblastoma cells (SHSY5Y), and hepatoma cells (HepG2) were treated with a range of OA concentrations in the presence and absence of S9 fraction. MN induction was observed in leukocytes at all concentrations tested, and in SHSY5Y and HepG2 cells only at the highest concentration (1000 nM). In contrast, γH2AX analysis was only positive for HepG2 cells. Taking together these data, in addition to the comet assay results obtained in a previous study in this issue, OA was found to exert a either a clastogenic or aneugenic effect dependent upon the cell types examined.

Spiroimine Toxins in Complex with Nicotinic Acetylcholine Receptors: Structure and Dynamics

Macrocyclic spiroimine phycotoxins belong to an emerging class of chemical agents associated with marine algal blooms and shellfish toxicity. [1] Representative members of this family are gymnodimines, spirolides, pinnatoxins, pteriatoxins, and spiro-prorocentrimine. Gymnodimine A and 13-desmethyl spirolide C have been shown to be potent antagonists of nicotinic acetylcholine receptor (nAChR), and have prompted the development of new tools to detect these spiroimine toxins in shellfish and for the design of novel drugs. [2,3] Very recently, crystal structures of Acetylcholine Binding Protein complexed with gymnodimine A and 13-desmethyl spirolide C were solved, thus providing insight into the orientation and the conformation adopted by these ligands in the binding pocket and their interactions with neighbouring amino-acid residues. [3]In this work we have explored the interaction of several members of spiroimine toxins family with different nAChR subtypes. Given the lack of general methods for flexible docking of macrocyclic ligands, we have developed a two-step, general approach to circumvent this problem, and applied it specifically to the docking of macrocyclic spiroimines on nAChRs. Subsequent molecular dynamics studies of the resulting receptor-ligand complexes allowed us to identify the key interactions responsible for the high affinity and target selectivity experimentally determined for some of these phycotoxins.[1] J. Molgo, E. Girard, E. Benoit, “The cyclic imines: an insight into this emerging group of bioactive marine toxins” in: Phycotoxins: Chemistry and Biochemistry (Eds.: Y. H. Hui, L. M. Botana), Blackwell Publishing, 2007, pp. 319-355.[2] R. Kharrat, D. Servent, E. Girard, G. Ouanounou, M. Amar, R. Marrouchi, E. Benoit, J. Molgo, J. Neurochem., 2008 107, 952-963.[3] Y. Bourne, Z. Radic, R. Araoz, T. T. Talley, E. Benoit, D. Servent, P. Taylor, J. Molgo, P. Marchot, Proc. Natl. Acad. Sci. USA, 2010, 107, 6076-6081.