Bioluminescence and toxicity as driving factors in harmful algal blooms: Ecological functions and genetic variability

Abstract

Dinoflagellates are an ecologically important group of marine microbial eukaryotes with a remarkable array of adaptive strategies. It is ironic that two of the traits for which dinoflagellates are best known, toxin production and bioluminescence, are rarely linked when considering the ecological significance of either. Although dinoflagellate species that form some of the most widespread and frequent harmful algal blooms (HABs) are bioluminescent, the molecular and eco-evolutionary associations between these two traits has received little attention. Here, the major themes of biochemistry and genetics, ecological functions, signaling mechanisms, and evolution are addressed, with parallels and connections drawn between the two. Of the 17 major classes of dinoflagellate toxins, only two are produced by bioluminescent species: saxitoxin (STX) and yessotoxin. Of these, STX has been extensively studied, including the identification of the STX biosynthetic genes. While numerous theories have been put forward as to the eco-evolutionary roles of both bioluminescence and toxicity, a general consensus is that both function as grazing deterrents. Thus, both bioluminescence and toxicity may aid in HAB initiation as they alleviate grazing pressure on the HAB species. A large gap in our understanding is the genetic variability among natural bloom populations, as both toxic and non-toxic strains have been isolated from the same geographic location. The same applies to bioluminescence, as there exist both bioluminescent and non-bioluminescent strains of the same species. Recent evidence demonstrating that blooms are not monoclonal events necessitates a greater level of understanding as to the genetic variability of these traits among sub-populations as well as the mechanisms by which cells acquire or lose the trait, as sequence analysis of STX+ and STX- species indicate the key gene required for toxicity is lost rather than gained. While the extent of genetic variability for both bioluminescence and toxicity among natural HAB sub-populations remains unknown, it is an area that needs to be explored in order to gain greater insights into the molecular mechanisms and environmental parameters driving HAB evolution.