The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health

Abstract

The dinoflagellate genus Alexandrium is one of the major harmful algal bloom (HAB) genera with respect to the diversity, magnitude and consequences of blooms. The ability of Alexandrium to colonize multiple habitats and to persist over large regions through time is testimony to the adaptability and resilience of this group of species. Three different families of toxins, as well as an as yet incompletely characterized suite of allelochemicals are produced among Alexandrium species. Nutritional strategies are equally diverse, including the ability to utilize a range of inorganic and organic nutrient sources, and feeding by ingestion of other organisms. Many Alexandrium species have complex life histories that include sexuality and often, but not always, cyst formation, which is characteristic of a meroplanktonic life strategy and offers considerable ecological advantages. Due to the public health and ecosystem impacts of Alexandrium blooms, the genus has been extensively studied, and there exists a broad knowledge base that ranges from taxonomy and phylogeny through genomics and toxin biosynthesis to bloom dynamics and modeling. Here we present a review of the genus Alexandrium, focusing on the major toxic and otherwise harmful species.

Figure 1

Phylogenetic tree inferred by maximum likelihood analysis of partial LSU rDNA (D1–D2 domains) of 21 nominal species of Alexandrium. Analysis includes a subset of taxa included in the maximum likelihood phylogenetic analysis of 28S rDNA by Touzet et al. (2008a). This analysis was supplemented by additional sequences for some species (or ribotypes of species complexes) from previous phylogenetic studies: A. pseudogonyaulax (MacKenzie et al., 2004), A. tropicale and A. minutum ‘Pacific clade’ (Lilly et al., 2005), A. ostenfeldii (Kremp et al., 2009), A. tamutum (Montresor et al., 2004), A. fraterculus and A. taylori (John et al., 2003b), and A. tropicale and A. tamiyavanichi (Menezes et al., 2010). In addition, Pyrodinium bahamense sequences used in the analyses by Leaw et al. (2005) were included, as well as those of other gonyaulacoid dinoflagellates, to demonstrate monophyly of the genus Alexandrium. Prorocentrum minimum was set as the outgroup. Sequences were aligned with MAFFT v6.814b (Katoh and Kuma, 2002) in Geneious 5.4.4 and the TrN+G model of base substitution was determined according to the Akaike Information Criterion and the Bayesian Information Criterion as the optimal model with jModeltest (Posada, 2008). Maximum likelihood analyses were carried out with PhyML (Guindon and Gascuel 2003) in Geneious 5.4.4 with the following constraining parameters: base frequency (A= 0.26832, C= 0.15771, G= 0.25629, T= 0.31768), Transition/transversion ratio for purines: 2.267, Transition/transversion ratio for pyrimidines: 4.725, gamma distribution shape parameter (G= 0.755). Branch frequencies from 100 bootstrap replicates are given in percent at the respective nodes if >50%. The two subgenera Alexandrium and Gessnerium (light gray shaded) do not form reciprocal monophyletic clades. Species complexes, such as the A. tamarense species complex, contain non-reciprocal monophyletic clades according to morphologically determined taxa, which rather resemble evolutionary units with distinct biogeographical distributions and varying degrees of morphological plasticity. * Isolate was originally misidentified as A. tropicale (Lilly et al., 2007)

Figure 2

Distribution of Alexandrium species in the Mediterranean Sea, modified from Penna et al. (2008). Open circles represent the sampled stations. Colored circles, square, triangle, and diamond symbols represent the species found by Penna et al. (2008) or by other authors, as defined and based on nucleotide sequences and morphology (see Section 2.3). Alexandrium andersoni ( ), A. minutum ( ), A. tamutum ( ), A. peruvianum/A. ostenfeldii ( ), A. insuetum ( ), A. margalefi ( ), A. pseudogonyaulax ( ), A. taylori ( ), A. affine ( ), A. catenella Group VI (◆), A. tamarense Group II ( ), and Group III ( ).

Figure 3

Schematic representation of the life cycle of heterothallic Alexandrium species. Species have a haplontic life cycle, i.e. the motile vegetative cells (1) are haploid. Under specific conditions, usually related to stress, some vegetative cells can transform into a non-motile pellicle cyst (2) that can rapidly switch back to the motile stage when conditions improve. The sexual phase starts with the formation of gametes (3), which conjugate (4) and form a diploid planozygote (5). Depending on environmental conditions, the planozygote can transform into a resting cyst (hypnozygote (6) or, for some species, can undergo meiosis and produce a vegetative cell (1). Cysts can spend variable periods of time in the sediments and, upon germination, release a motile cell