Gymnodinium and Related Dinoflagellates

Abstract

Mounting molecular evidence and ultrastructural differences, in particular the type of apical groove and flagellar apparatus architecture, have provided sufficient evidence over the past decade to demand a revision of the dinoflagellate genus Gymnodinium, as it contained a complex assemblage of evolutionarily unrelated species. Consequently, the genus has now been split into four genera: Gymnodinium, Akashiwo, Karenia and Karlodinium. The only remaining harmful species within the genus Gymnodinium is Gymnodinium catenatum, a species that causes paralytic shellfish poisoning, and it was recently introduced into Australian waters via ship ballast water. The genus Akashiwo contains no toxic representatives, whilst the genera Karenia and Karlodinium are close sister lineages with both genera incorporating ichthyotoxic species. Many representatives form blooms and produce toxins thus providing valuable insight into fundamental phylogenetic and biochemical questions. Taxa assigned to these genera are known to be toxin producers of extreme importance to biomedicine.

Key Concepts:

  • Molecular data have led to substantial changes of classifications within the protists, to which the dinoflagellates belong.

  • Consequently, names of genera and species have changed many times, resulting in taxonomic confusion, particularly for researchers working in the field of ecology or environmental monitoring.

  • The former genus Gymnodinium has long been recognised to be polyphyletic.

  • Molecular data and ultrastructural details, such as the type of apical groove and flagellar apparatus architecture, have resulted in a reclassification of the former genus Gymnodinium.

  • Taxonomic revision resulted in splitting the former genus Gymnodinium into four genera: Gymnodinium, Akashiwo, Karenia and Karlodinium.

  • Additional revision of the genus Gymnodinium sensu Daugbjerg et al. (2000) might be necessary, which would transform the very large and species‐rich former genus Gymnodinium into one of the smallest.

  • Irrespective of the reclassification, many of the organisms within these four genera form harmful algal blooms and produce toxins that can affect invertebrates, lead to fish mortality and can severely affect human health.

  • Some of the toxins produced have been used successfully in biomedical research, which helped to elucidate the mechanisms that control operation of the voltage‐gated sodium channel.

  • Blooms by these organisms lead to large economic losses for shellfish aquaculture, in particular blooms by Gymnodinium catenatum, whose toxins induce paralytic shellfish poisoning, which may result in human death.

  • The expansion of the aquaculture industry, shellfish and fish trades around the globe, and climate change‐induced range expansions, as well as introduction via ships’ ballast water to nonendemic areas require an efficient monitoring system for dinoflagellate toxins and harmful algal blooms.

Keywords: dinoflagellate; Gymnodinium; Karenia; Akashiwo; Karlodinium; toxic algae; voltage‐gated sodium channels; harmful algal blooms; flagellar apparatus ultrastructure; apical groove

Figure 1.

Scanning electron micrograph of Karenia brevis – the causative organism of ‘red tide’ and neurotoxic shellfish poisoning on the Florida coast of the Gulf of Mexico.

Figure 2.

(a) Model showing the arrangement of basal bodies relative to one another throughout the dinoflagellates. Gymnodinium and allied genera typically possesses basal body angles between 90° and 180°. (b) Diagrammatic reconstruction of a generalised gymnodinioid flagellar apparatus bearing a large ventral connective fibre.

Figure 3.

(a) Chemical structure of saxitoxin and natural derivatives produced by Gymnodinium catenatum (modified from Falconer, ). These toxins cause paralytic shellfish poisoning (PSP). The toxicity of the groups decreases from the carbamate toxins to decarbamoyl toxins and the N‐sulfocarbamoyl toxins. The decarbamoyl toxins are metabolic conversions of the other two groups. These toxins are water‐soluble and heat‐resistant and are known specifically to block voltage‐gated sodium channels by interacting with site 1 (Figure ). Both the guanidinium group and hydroxyl groups have been strongly implicated in the specific recognition of sodium channels (Falconer, ). The dihydroxy ketone group on the five‐membered ring is essential for toxicity as shown by loss of activity upon catalytic reduction of this group to a monohydroxy group (Halstead and Schantz, ). (b) Chemical structure of brevetoxin and some derivatives produced by Karenia brevis (modified from Falconer, ). The polyether toxins (PbTx‐1 and PbTx‐2‐type), also known as brevetoxins A and B, cause neurotoxic shellfish poisoning (NSP) and are lipid‐soluble. In contrast to the saxitoxins, brevetoxins specifically bind to site 5 on the α subunit of the voltage‐gated sodium channel (Figure ). The H–I–J–K ring topography is essential for binding and the A‐ring lactone moiety contributes to binding and toxicity. The binding of brevetoxin to voltage‐gated sodium channels opens them at the resting membrane potential and inhibits the inactivation, thus causing membrane depolarisation and repetitive firing (Falconer, ). STX, saxitoxin; GTX, gonyautoxin; dc, decarbamoyl.

Figure 4.

Model of a voltage‐gated sodium channel and the interaction of gonyautoxin (11‐hydroxy‐saxitoxin) and brevetoxin. The voltage‐gated sodium channel consists of one large polypeptide that is folded in such a way that hydrophobic regions interact with the membrane and the hydrophilic regions form a sodium‐specific pore. At the resting potential of –70 mV, the membrane is polarised and the channel is closed (stage I). Upon a stimulus, the membrane depolarises to +50 mV and the channel opens (stage II). The depolarisation of a particular part of the membrane leads to subsequent depolarisations, opening sodium channels further down the track and thus amplifying and passing on the signal in a muscle or nerve membrane. Spontaneous conformational changes of the open sodium channels, at a membrane potential where they would normally be open, effectively regulates sodium fluxes. This is referred to as an inactivated sodium channel (stage III). This step is necessary to repolarise the membrane and close the channel properly to allow for the next round of stimulus‐coupled membrane depolarisation and channel opening. Guanidinium is a cation substitute for sodium in generating action potentials and it thus has been proposed that the positively charged guanidinium group of saxitoxins/gonyautoxins enters the channel to interact with the ion‐selective pore. These toxins interact with closed, open and inactive sodium channels, and require the presence of the α and β1 subunits of the channel. The sodium influx blocking action of these toxins is restricted to the interaction with the external face of the sodium channel. Upon binding, the bulky toxin would then sterically block the passage of sodium ions through this narrow ion‐selective pore (for review, see Falconer, ). As the inward flow of sodium is blocked, a received stimulus at the membrane will not lead to the normal subsequent effects of action potential propagation (stages II and III). Thus, these toxins exhibit a relaxant effect on vascular smooth muscle and the rate of rise and amplitude of action potentials are depressed in cardiac muscle (Falconer, ). Hence, these toxins can, in sufficient quantities, cause death by respiratory distress and muscle paralysis. Brevetoxins are neurotoxins that cause neurotoxic shellfish poisoning (NSP) and massive fish kills (Falconer, ). In contrast to the saxitoxins, the polyether toxins (brevetoxins) bind to a different epitope on the α subunit of the voltage‐gated sodium channel, known as site 5. The point of interaction between the toxins and the α subunit has been identified using a photolabelled brevetoxin derivative, followed by antibody mapping of proteolytic fragments of the channel with the bound toxin. The toxins are believed to specifically alter the conformation of the voltage‐gated sodium channel, thus opening it at a negative membrane potential, when it would normally be closed, and also inhibit the conformational change that inactivates the channel. This allows sodium influx, which leads to depolarisation of nerve and muscle membranes and spontaneous, repetitive action potentials.

Figure 5.

Flow chart describing monitoring programmes to minimise human poisoning and indirect effects on human health. It is apparent that in countries with no monitoring programmes (NO), human health is severely and directly endangered affecting more people and there is an increased risk of poisoning‐induced fatalities. Even when appropriate monitoring programmes are in place (YES), human health may still be indirectly affected due to stress‐related illnesses. Appropriate combinations of different monitoring systems will, however, minimise poisonings due to ingestion of toxic fish/shellfish and hence the risk of fatalities.

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Heimann, Kirsten(Mar 2012) Gymnodinium and Related Dinoflagellates. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001967.pub2]