Evolution and distribution of saxitoxin biosynthesis in dinoflagellates

Abstract

Numerous species of marine dinoflagellates synthesize the potent environmental neurotoxic alkaloid, saxitoxin, the agent of the human illness, paralytic shellfish poisoning. In addition, certain freshwater species of cyanobacteria also synthesize the same toxic compound, with the biosynthetic pathway and genes responsible being recently reported. Three theories have been postulated to explain the origin of saxitoxin in dinoflagellates: The production of saxitoxin by co-cultured bacteria rather than the dinoflagellates themselves, convergent evolution within both dinoflagellates and bacteria and horizontal gene transfer between dinoflagellates and bacteria. The discovery of cyanobacterial saxitoxin homologs in dinoflagellates has enabled us for the first time to evaluate these theories. Here, we review the distribution of saxitoxin within the dinoflagellates and our knowledge of its genetic basis to determine the likely evolutionary origins of this potent neurotoxin.

Figure 1

The three theories of saxitoxin (STX) evolution in dinoflagellates: (1) Co-cultured bacteria: Intracellular bacteria associated with the dinoflagellate cell are synthesizing STX; (2) Convergent evolution: The independent evolution of an analogous STX product in cyanobacteria and dinoflagellates (black dotted arrows); (3) Horizontal gene transfer (HGT): STX evolved in dinoflagellates after a single HGT event with cyanobacteria (red dotted arrow). The dinoflagellate and cyanobacterial lineages are highlighted in red rectangles. For illustrative purposes, the Kingdom Archaea, is collapsed. Eukaryotic [8] and bacterial [9] lineages are collapsed at different taxonomic levels.

Figure 2

The evolution of the dinoflagellates, Alexandrium, and the distribution of STX, our present understanding: Only the “core” dinoflagellates are represented (to the left), with clades collapsed at different taxonomic levels [51]. The Alexandrium genus [15] is expanded (to the right). Red font: STX⁺ species. Blue font: STX⁻ Alexandrium species. SxtA [22,23,51,55,56] and sxtG [23,28] presence or absence is highlighted to the right of the name. The sxtG box for A. ostenfeldii and A. tamiyavanichi is blank, as they remain to be tested [55,56]. The HGT events are defined “1” and “2”, representing a primary and secondary HGT/EGT, respectively.