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«Chapter 2 Biological Toxins from Marine and Freshwater Microalgae Antonino Santi Delia, Gabriella Caruso, Lucia Melcarne, Giorgia Caruso, Salvatore ...»

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Chapter 2

Biological Toxins from Marine

and Freshwater Microalgae

Antonino Santi Delia, Gabriella Caruso, Lucia Melcarne,

Giorgia Caruso, Salvatore Parisi and Pasqualina Laganà

Abstract

In the last decades the increased occurrence of intoxications caused by

biological toxins produced from marine and freshwater microalgae has underlined

their relevance as emerging risks for food safety. Biological toxins from algae (i.e.

saxitoxin, brevetoxin, okadaic acid, domoic acid) are recognised as a major threat for human and animal health, especially where Harmful Algal Blooms phenomena develop. Many of these toxins are responsible for severe illness or death, mostly related to consumption of seafood contaminated by toxic algae. The present book summarises current knowledge and perspectives for future research on marine and freshwater algal toxins. Specific topics are: overview of the different species producing toxins, their survival strategies in the environment; typologies of toxins, their chemical structure and mechanisms of actions; methods currently in use for their monitoring; emerging issues and future outlooks for their control. The importance of biotoxin monitoring in the framework of the European Marine Strategy Framework Directive is also discussed.

Á Á Á Á Keywords Brevetoxin Ciguatoxin Cylindrospermopsin Domoic acid Harmful Á Á Á Á Á algal bloom Microcystin Okadaic acid Poisoning Saxitoxin Yessotoxin Abbreviations ASP Amnesic Shellfish Poisoning AOAC Association of Official Analytical Chemists AZA Azaspiracid AZP Azaspiracid Shellfish Poisoning β-Methylamino-L-Alanine BMAA PbTx Brevetoxin CYN Cylindrospermopsin BIOTOX Development of Cost-Effective Tools for Risk Management and Traceability Systems for Marine Biotoxins in Seafood DSP Diarrhetic Shellfish Poisoning DST Diarrhetic Shellfish Toxin DiCANN Dinoflagellate Categorisation by Artificial Neural Network DTX Dinophysistoxin © The Author(s) 2015 13 G. Caruso et al., Microbial Toxins and Related Contamination in the Food Industry, Chemistry of Foods, DOI 10.1007/978-3-319-20559-5_2 14 2 Biological Toxins from Marine and Freshwater Microalgae DA Domoic Acid ELISA Enzyme-Linked ImmunoSorbent Assay EFSA European Food Safety Authority EU European Union GEOHAB Global Ecology and Oceanography of Harmful Algal Blooms GES Good Environmental Status HAB Harmful Algal Bloom HPLC High-Performance Liquid Chromatography LD50 Median Lethal Dose

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2.1 Toxin-Producing Microorganisms 2.1.1 Generalities on Phytoplankton and Toxic Species:

Spatial and Temporal Distribution—Environmental Drivers Phytoplankton comprises unicellular or colonial, microscopic organisms (microalgae) that inhabit many aquatic ecosystems. Algae are autotrophic organisms, which are able through the photosynthetic process to convert carbon dioxide and water

2.1 Toxin-Producing Microorganisms 15 into sugars for the cell metabolism, using the energy from sunlight. They are subdivided into 10 groups (Bold and Wynne 1985): Cyanophyta, Prochlorophyta, Chlorophyta, Charophyta, Euglenophyta, Phaeophyta, Chrysophyta, Pyrrophyta, Rhodophyta, Cryptophyta and another group including other species.

Within the planktonic food web, phytoplankton occupies the first trophic level with a key role as primary producer of organic matter. The phytoplankton community inhabiting aquatic environments undergoes seasonal changes characterised by the succession of different unicellular or colonial taxa (Bruno 2000).

The temporal variability in the composition of the phytoplankton community is associated with spatial variability. Along the water column, phytoplankton species are differently distributed depending on the different tolerance of their photosynthetic pigments to light wavelength spectra and on the ability to move towards zones more enriched in nutrients. Cyanophyceae are more frequent on surface layers as their coloured pigments protect chlorophyll from ultraviolet (UV) denaturation, while Dinoflagellates inhabit shallow, weakly lighted, environments. At intermediate depths, Chlorophyceae are dominant with the exception of lakes in spring and autumn, and spring waters where Crysophyceae are prevalent.

Close to the thermocline layer, Diatoms predominate.

Of the approximately 5,000 species of identified microalgae, about 300 are able to develop under massive growth, producing ‘red-water’ phenomena, whose occurrence was reported thousands of years ago. In some cases, the proliferation of planktonic algae (the so-called ‘algal bloom’) is a real benefit for aquaculture. Many species can create extended marine algal blooms named ‘red tides’: sometimes, they do not constitute a hazard to human health. Red tides are produced when layers of deep water, rich in nutrients, overlap layers of warmer surface water, due to solar heating or due to surface freshwater supplies. In eutrophic environments, algal blooms involve one or two phytoplanktonic species, which represent 80–90 % of the total biomass. In oligotrophic environments, seasonal blooms also occur but they are never mono-specific. These phenomena occur when warmer surface water overlaps deeper water rich in nutrients; under these conditions, rapidly growing algae consume nutrients from the surface waters, leaving those present under the pycnocline. Motile algae arrive to this layer, where they produce blooms that move towards the surface during the day to capture light and heat (Bruno 2000). Algal species quickly exhaust the nutrients of the surface layers with a rapid growth, leaving those in the colder layer below the pycnocline.





Some algae species such as Dinoflagellates, able to migrate vertically even with higher speeds of 10 m/day, can reach this layer where they find optimal conditions of temperature and nutrients for their growth. Those algal species that can compete successfully for available growth-limiting nutrients have the potential to become dominant and produce blooms (Granéli et al. 2008). In some cases, however, algal blooms are recognised dangerous agents because of the ability of modifying the visual appearance of water. In addition, they can be considered foam-producing organisms and able to cause toxic effects, with possibility of death, on the human population and fish (ICES 1984). For these reasons, these life forms are considered Harmful Algal Blooms (HAB). An approximate number of 75 species, mostly 16 2 Biological Toxins from Marine and Freshwater Microalgae represented by dinoflagellates and diatoms, inhabit both marine and freshwater ecosystems. They are recognised as toxic substance producers since they produce biotoxins (phycotoxins) that include the most powerful non-protein toxins known to date. In fact, the blooms of toxic microalgae occurring on the coasts have been responsible for die-offs of wild animals, livestock and pets. The consumption of shellfish, fish or water contaminated by algal toxins has been associated with very serious cases of poisoning in humans and negative effects on aquatic environments.

According to the produced effects, the species involved in outbreaks of toxic

algal blooms can be distinguished in three main groups (Bruno 2000):

• 1st group. Species that cause water colouration only, resulting in a decrease of the water transparency, and which may exceptionally grow causing some episodes of fish and invertebrate mortality, related to oxygen consumption during their decomposition. Species of dinoflagellates and diatoms belong to this group • 2nd group. Species which produce powerful toxins that accumulate along the trophic web and can cause effects in upper consumers (animals and humans);

dinoflagellates belonging to Alexandrium, Gymnodinium, Dinophysis, Prorocentrum and diatoms belonging to the genus Pseudo-nitzschia are included in this group • 3rd group. Species that are not toxic to humans but are noxious to fish and invertebrates (i.e. Gyrodinium aureolum, Chaetoceros convolutus, Nodularia spumigena, Chattonella spp). In addition, some toxic species spread their toxins through the production of aerosols reaching the coasts (i.e. Gymnodinium breve and Ostreopsis spp).

Phytoplankton life forms can cause many problems in Europe and worldwide (Anderson 1989). This bloom results in severe economic and sanitary consequences when waters are used for recreational and productive purposes (tourism, fisheries and aquaculture). Algal toxins have negative impacts on the health of marine organisms, such as fish, shellfish and crustaceans; moreover, they are concentrated in seafood products through water filtration mechanisms and become dangerous to human health when contaminated seafood are consumed. Negative impacts and correlated mechanisms are extremely different. Many of these impacts are characterised by chemical–ecological interactions mediated by secondary metabolites of various bioactivity, as shown by their diverse structural classification and the range of receptors and metabolic processes affected (Cembella 2003). Many biologically-active molecules, including dangerous toxins for animal life, can be chosen as good indicators (Codd 2000). Toxic microalgae are common only among the dinoflagellates, diatoms and cyanobacteria (Katircioǧlu et al. 2004).

In marine environments, the division of Pirrhophyta includes the greatest number of algal species currently known as producers of toxins or harmful substances: two classes of Dinophyceae and Desmophyceae are considered. The toxic species such as Dinophysis, Gymnodinium, Peridinium and Gonyaulax belong to the class of Dinophyceae, while Prorocentrum belongs to the class of Desmophyceae. Many toxins are produced by dinoflagellates, but also some diatoms are also toxic.

2.1 Toxin-Producing Microorganisms 17 In freshwater environments, toxic algal species mostly belong to Cyanophyceae.

They are a well-defined group of prokaryotic organisms, concerning about 150 genera and over 2000 species (van den Hoek et al. 1995). These algae have a photosynthetic apparatus similar in structure and function to that of chloroplasts of eukaryotes, thanks to the presence of chlorophyll a responsible for oxygenic photosynthesis. Cyanophyceae show a great diversity in morphology, structure and functions, and phenotypes; these species are represented by complex populations (ecotypes) which express particular genotypes. The toxic species are about 40; the ability to produce toxins has an important taxonomic significance (Skulberg and Skulberg 1985).

Cyanophyceae are ubiquitous organisms present in aquatic environments with wide salinity ranges and temperature up to 73–74 °C, in soil, in rocks; some genera are able to fix atmospheric nitrogen through heterocysts and members of symbiotic relationships. Many filamentous and unicellular species are motile, through mucilage or filaments. Cytoplasm shows some gas vacuoles that regulate their floating over water surface. There are three orders: Chroococcales, Chamaesiphonales, Oscillatoriales; the first and the third include some toxin-producing species.

Many species belonging to Cyanobacteria are responsible (O’Neil et al. 2012) for HAB in freshwater, estuarine and marine environments. The incidence of cyanobacterial blooms has been observed with high results in different aqueous environments (Carmichael 2008; Paerl 2008; Paerl and Huisman 2008; Paul 2008).

Some new cyanobacterial toxins, such as β-methylamino-L-alanine (BMAA), have been isolated, as well as new genera of toxin-producing cyanobacteria (Brand 2009;

Cox et al. 2005, 2009; Kerbrat et al. 2011).

2.1.2 Major Toxic Algal Species: An Overview 2.1.2.1 Diatoms—Pseudo-nitzschia spp Pseudo-nitzschia was observed with other diatom species in certain Italian and Spanish areas (Quijano-Scheggia et al. 2005; Totti et al. 2000). The production of toxin (domoic acid) was found in different Mediterranean areas (Azmil et al. 2001;

Kaniou-Grigoriadou et al. 2005), possibly in association with two Pseudo-nitzchia microrganims (Cerino et al. 2005; Orsini et al. 2002).

The abundance and distribution of toxic Pseudo-nitzschia species (particularly P. calliantha and P. delicatissima, two potential ‘Amnesic Shellfish Poisoning’ toxin producers) was studied in Italian waters (Caroppo et al. 2005). P. calliantha showed a stronger seasonal distribution and was correlated with winter water conditions than P. delicatissima, which in turn exhibited a broader temporal distribution and appeared independent from major environmental constraints. Pseudo-nitzschia spp have been detected in diverse environments such as high-nitrate and low-chlorophyll regions (open ocean), but also in fjords, gulfs and bays; the same thing may be observed when speaking of produced toxins because of the well known stability.

18 2 Biological Toxins from Marine and Freshwater Microalgae 2.1.2.2 Dinoflagellates Alexandrium spp The genus Alexandrium, including the species A. minutum, A. catenella, A. tamarense and A. taylori, is recognised to be responsible for different toxic episodes in many Mediterranean areas (Giacobbe et al. 2007; Penna et al. 2005; Vila et al.

2001, 2005).

Basically, Alexandrium is well known because of repeated observations in many different ecosystems (Anderson et al. 2012a). In addition, the specificity of Alexandrium species is correlated with the production of three different toxin groups, in spite of the multiplicity of nutritional exigencies. By the hygienic viewpoint, Alexandrium blooms have been considered as one of the most important topics when speaking of HAB-related toxin episodes. As a result, a notable amount of scientific literature is available at present with relation to different aspects, including also effects on the environment.

Dinophysis spp

Being a cosmopolitan genus, Dinophysis spp has been considered as one of the main problems for shellfish aquaculture in many European Countries and other regions because of the production of okadaic adic and pectenotoxins, powerful lipophilic toxins. The first report on Dinophysis species concerned (Caroppo et al.

2001) the composition and spatio-temporal distribution in the oligotrophic waters of the southern Adriatic coasts (Apulia, Italy).



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