Alexandrium is a genus of dinoflagellates. It contains some of the dinoflagellate species most harmful to humans, because it produces toxic harmful algal blooms (HAB) that cause paralytic shellfish poisoning (PSP) in humans. There are about 30 species of Alexandrium that form a clade, defined primarily on morphological characters in their thecal plates.Murray, S.A., John, Uwe., Kremp, Anke. (2015): Alexandrium spp: genetic and ecological factors influencing saxitoxin production and proliferation. Climate Change and Marine and Freshwater Toxins. 123–139.
Introduction The group was not well-defined in the past and thus, due to interest of its toxic behaviour, people have revised the group through formal tabulation and usage of molecular markers such as the toxic gene, stx4A, to better understand not just the relationship between each species; but more importantly, to tell something about the spread and barriers to the bloom. Even if, much is known about the life cycles related to the blooms, much is still unknown as to how each life stage is triggered and transitions to the next stage. Predation and parasitism have proven to be great barriers for population growth. Learning about the pathways of toxin synthesis can allow us to determine how species of Alexandrium have adapted and co-evolved to persist.Anderson, D.M., Alpermann, T.J., Cembella, A.D., Collos, Y., Masseret, E., Montresor, M. 2012: The globally distributed genus Alexandrium: Multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae. 14(2012): 10–35. https://dx.doi.org/10.1016/j.hal.2011.10.012
Etymology In the 1960s, an Egyptian researcher by the name of Youssef Halim discovered a red tide along the coast of the Alexandria harbour in Egypt. It was the first described red tide in Egypt and later on, Halim identified and named the culprit as Alexandrium as homage to where it was found and he identified Alexandrium minutum as the genus's type species.Halim, Y., 1960. Alexandrium minutum n. gen. n. sp., dinoflagellé provocant “des eaux rouges”. Vie et Milieu, 11, 102–105.Balech, Enrique. 1995: The Genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine Station, Sherkin Island, Co., Cork, Ireland.
History of knowledge Species currently included in Alexandrium have been known for a long time, but initially they were classified in different genera, notably, Gonyaulax. Nonetheless, the first attempt at revising the genus, Gonyaulax, was made by Kofoid in 1911. Kofoid was a very influential biologist during his time. His greatest work was the development of the universal "Kofoid System" that classified dinoflagellates based on plate morphology very detailed drawings and well-defined structures. Unfortunately, however Kofoid divided Gonyaulax into four subgenera based on shape, and included several species that should not have been classified under the name Gonyaulax.
Lebour (1925) described a new species called Gonyaulax tamarensis.Lebour, M.V., 1925. The dinoflagellates of northern seas. Marine Biological Association of the United Kingdom, Plymouth, p. i–vi, 1–250, 35 pl. Whedon and Kofoid in 1936 used the same tabulation as Lebour and described two new species, Gonyaulax acatenella and Gonyaulax catenella.Whedon, W.F., Kofoid, C.A., 1936. Dinoflagellata of the San Francisco region. I. On the skeletal morphology of two species, Gonyaulax catenella and G. acatenella. University of California Publications in Zoology 41(4), 25–34. The latter was studied in much more detail due to the fact that it caused paralytic shellfish poisoning (PSP) in humans, who acquire it from bivalve mollusks. As more and more species were described, they either put them into the "tamarensis group" or the "catenella group". By no means was it simple to put species into either group and this caused great confusion. The "tamarensis group" was divided into two subgroups and were separated by whether or not one of its thecal plates had contact with the ventral pore or not. Goniodoma and Gonyaulax were very similar. In 1954, Gaarder stated that her Goniodoma species described had very similar characteristics to the "tamarensis group" in Gonyaulax.Gaarder, K.R., 1954a. Dinoflagellates from the Michael Sars North Atlantic Deep-Sea Expedition 1910. Report on the Scientific Results of the „Michael Sars“ North Atlant. Deep-Sea Exped. 1910, University of Bergen, John Grieg, Bergen 2(3), 1–62 + Tabl. 1–5. She is believed to be the first to clarify the differences in the two groups based on the plate tabulation.
In 1960, Halim created the new genus Alexandrium with Alexandrium minutum as the only species described in it and he put it into the "tamarensis group". The "tamarensis group" had become a taxonomical chaos by this time, in part because many scientists had differences in opinion about the species and genus taxonomy included in this group. Many species from the same location had been given several names. The group included for example the genus: Gonyaulax, Goniodoma, Pyrodinium, Alexandrium, Gessnerium, Protogonyaulax, and Glenodinium. In 1971, the group was revised by Steidinger, who suggested that the "tamarensis group" should be separated from Gonyaulax. She also recognized Alexandrium as being part of the group. Meanwhile, in the same year, Balech suggested that the Gonyaulax group should be separated into Alexandrium or Gessnerium.
What gave people interest in studying Alexandrium was because it produces paralytic shellfish toxins (PST). The theory of becoming toxic was that originally, bacteria in the ocean would compete with each other producing toxic by-products. Alexandrium being bacterivorous would ingest these bacteria and gain the ability to produce these PST's. Later studies have shown that indeed if you remove the symbiotic bacteria of specific Alexandrium species, the dinoflagellate produces less toxin. If you put new bacteria into the Alexandrium species, there is no change in toxin production.Gallacher, S., Smith, E.A. 1999: Bacteria and Paralytic Shellfish Toxins. Protist. 150: 245–255. https://dx.doi.org/10.1016/S1434-4610(99)70027-1 Nonetheless, this theory needs more evidence to be supported.
Molecular phylogeny Before molecular data, the main way to distinguish between Alexandrium species was to identify whether or not it made chains or if the 1' thecal plate touched the ventral pore or not. (5) However, this was not very effective in distinguishing between different species, especially, as more and more species were described. Hence, taxonomists have organized different species into different species complexes based on gene markers, of which the two most well-established and deadliest ones are the Alexandrium tamarense species complex and the Alexandrium minutum species complex.
Originally, the Alexandrium tamarense species complex included Alexandrium tamarense, Alexandrium fundyense, and Alexandrium catenella. The phylogeny was created using primarily Large Subunit and Small Subunit ribosomal RNA. By constructing using rDNA, researchers found that the phylogeny forms five different geographical clades in the Alexandrium tamarense species complex. These are the North American, Western European, Temperate Asian, Tasmanian, Tropical Asian clades, and a Mediterranean clade.Gu, H., Zeng, N., Liu, T., Yang, W., Muller, A., Krock, B. 2013: Morphology, toxicity, and phylogeny of Alexandrium (Dinophyceae) species along the coast of China. Harmful Algae. 27(2013): 68–81. https://dx.doi.org/10.1016/j.hal.2013.05.008
The new revised Alexandrium tamarense species complex is grouped into five clades that are named Groups I-V. There are currently 5 species included in this complex: Alexandrium fundyense (Group I); Alexandrium mediterraneum (Group II); Alexandrium tamarense (Group III); Alexandrium pacificum (Group IV); Alexandrium australiense (Group V).Lilly, E.L., Halanych, K.M., and Anderson, D.M. 2005: Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae. 4(2005): 1004–1020.
There are three morphospecies that can be distinguished primarily based on morphology: A. catenella, A. fundyense, and A. tamarense. They have differences in their size (length to width ratio), the presence or absence of the ventral pore attached to the 1' or even the 4' thecal plate, and the differences in other thecal plates. A. catenella can form chains, while A. fundyense and A. tamarense cannot. A. catenalla has a lower length to width ratio than the other two. (5) A. tamarense has a ventral pore, but the other two do not. It has been found that many cells have intermediate morphologies between the morphologies described in A. tamarense and A.fundyense. As well, the ventral pore was sometimes present and sometimes absent in A. fundyense. Although A. catenella is found in the same location as A. fundyense, it is suggested to not include it in the Alexandrium tamarense species complex. Morphological characteristics have been less distinctive than scientist have originally thought.
However, using rDNA has provided more confidence on differentiating them phylogenetically. Using ITS/5.8S genetic distances within and between species, one can differentiate between differences in genomic mismatch between the two species. The genetic distance between the same species was much lower than between different species confirming the distinct species-specific clades. ITS2 compensatory base changes (CBC) are used as genetic markers that is used for studying the diversity of eukaryotic species. CBC in the secondary structure of helix III are present in groups I, II, and V, but absent in groups III and IV. Groups I and III cannot produce viable cysts. Scientists screened for presence or absence of the domain of the gene to determine the toxicity of each group. Groups I and IV produce saxitoxin, while groups II and III do not. Group V can sometimes produce or not produce saxitoxin. There are several other species that are not included in this group.
Alexandrium minutum species complex includes A. lusitanicum, A. angustitabulatum, A. minutum, A. andersonii, A. tamutum, and A. insuetum. The main difference between this group and the tamarense species complex, is that the A. minutum group species are much smaller and the development of toxicity is much variable, even between different strains. Again, previously this group was defined based on morphology. But the morphology of this group is much more variable, especially in the different strains. A. insuetum was the only species that did not have the 1' plate connected to the ventral pore. Both A. angustitabulatum and A. lusitanicum were very similar in morphology to A. minutum. A. andersonii was the most different from the group and was slightly larger than the average size of the group. A. tamutum is also similar to A. minutum but has a wider 6' plate. Upon new morphological analysis, it was shown that there was no difference between the width of the s.a. plate and the 1' plate which was thought to have been the same in the past.