New insights on the ecophysiology and ichthyotoxicity of the dinoflagellate Alexandrium catenella from Chilean fjords

Harmful Algal Blooms (HABs) are common natural phenomena along the Chilean coast. In southern fjords, the dinoflagellate Alexandrium catenella is the most studied species because of its production of saxitoxin and analogues responsible for Paralytic Shellfish Poisoning (PSP). Despite its deleterious effects on the local shellfish and finfish aquaculture industry, little is known about the dinoflagellate's ecology in this complex fjord ecosystem. In the present study in vitro experiments were conducted to determine: i) the role of A. catenella resting cysts in bloom dynamics; ii) physiological response of vegetative cells to `pCO_2``/pH` variations; and iii) the cytolytic potency of its exudate compounds against fish gill cells. Cyst experiments newly revealed a short cyst dormancy period (minimum 69 days) and highly variable reproductive compatibility determined by the geographical origin of isolates and their population genetic distances. Excystment processes were strongly driven by environmental factors, such as salinity and irradiance, which therefore provide important clues to understand regional bloom events. These results suggest a more important role for resting cysts in bloom dynamics in the Chilean fjords than previously thought. Exposure of A. catenella to variations in `pCO_2``/pH` resulted in optimum growth and dissolved inorganic carbon (DIC) uptake at near equilibrium pH (8.0). Reduced cell size and enhanced chain formation occurred at high `pH``/low` `pCO2`. These results point to morphological and physiological adaptations by A. catenella against wide natural `pCO_2``/pH` fluctuations, and suggests a negligible impact of future ocean acidification scenarios on Alexandrium bloom dynamics in southern fjords. Our results on the potency of cytolytic toxins produced by A. catenella assessed on a rainbow trout gill cell line assay showed that pure PST fractions (C1&C2, STX, GTX 1&4) had insignificant lytic activity compared to the synergistic interaction between reactive oxygen species (ROS) and polyunsaturated fatty acids (PUFA). The novel application of non-invasive microelectrode ion flux measurement (MIFE) techniques on fish gill cells revealed that A. catenella metabolites from lysed cultures affected gill cell `K^+` channels by generating a strong efflux from the cell membrane, but again this was not caused by PST fractions. Cellular potassium efflux is known to generate cell shrinkage and cell death, and might be a key factor to explain fish gill damage from A. catenella. This study newly elucidated key aspects of the ecophysiology and the fish-killing mechanisms of A. catenella in the Chilean fjords. These results have important implications for the way the salmon industry should manage and mitigate future algal bloom events.