Increased cellular brevetoxins in the red tide dinoflagellate Karenia brevis under CO2 limitation of growth rate: Evolutionary implications and potential effects on bloom toxicity

Abstract

Karenia brevis blooms impair human health, marine ecosystems, and coastal economies in the Gulf of Mexico via their production of carbon‐based neurotoxins (brevetoxins), which contain no nitrogen (N) or phosphorus (P). N and P limitation of growth rate substantially increases brevetoxins in this dinoflagellate, consistent with predictions of the carbon nutrient balance (CNB) hypothesis. This hypothesis further predicts that an increase in carbon‐based brevetoxins should not occur if growth rate is limited by carbon dioxide (CO2). We tested this prediction by examining the effect of CO2 limitation of K. brevis growth rate on cellular brevetoxins. In contradiction to the prediction of the CNB hypothesis, brevetoxins normalized to cell carbon were on average 81% higher in CO2‐limited cells growing at a rate of 0.1 d−1 than in cells growing at their maximum rates (0.4–0.5 d−1). This increase in brevetoxin : C values in the CO2‐limited cells, however, was 23–42% lower than that previously observed for comparable growth rate limitation by phosphate. The CO2‐limited cells also exhibited 40% higher cellular N : C and 60–100% higher chlorophyll a : C than observed in P‐limited cells at equivalent growth rates. These effects were likely due to the up‐regulation of the cell's CO2‐concentrating mechanism under CO2 limitation, which increased the demand for photosynthetically produced adenosine‐5′‐triphosphate. The results indicate that anthropogenic increases in CO2 concentrations in surface ocean waters are likely to increase the toxicity of K. brevis blooms due to potential increases in bloom biomass yield and to a greater likelihood that dense blooms will become N or P limited rather than CO2 limited.