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 (CO 2 ). We tested this prediction by examining the effect of CO 2 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 CO 2 -limited cells growing at a rate of 0.1 d 21 than in cells growing at their maximum rates (0.4-0.5 d 21 ). This increase in brevetoxin : C values in the CO 2 -limited cells, however, was 23-42% lower than that previously observed for comparable growth rate limitation by phosphate. The CO 2 -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 CO 2 -concentrating mechanism under CO 2 limitation, which increased the demand for photosynthetically produced adenosine-59-triphosphate. The results indicate that anthropogenic increases in CO 2 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 CO 2 limited.

Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton

“…Instead, as growth slowed under P limitation, cells down-regulated the rate of toxin synthesis, but to a lesser degree than the overall decrease in the rate of cellular C production leading to higher cellular toxin:C ratios. Similar increases in cellular brevetoxin:C ratios were also observed under both N limitation (Hardison et al 2013) and CO 2 limia-tion of growth rate (Hardison et al 2014), suggesting that the increase in brevetoxins is inherently linked to the slower growth rates that occur during nutrient limitation. Hardison et al (2012Hardison et al ( , 2013 hypothesized that the increase in cellular toxins is evolutionarily advantageous, as elevated brevetoxins have been shown to deter zooplankton grazing (Hong et al 2012).…”

“…) and CO 2 limiation of growth rate (Hardison et al. ), suggesting that the increase in brevetoxins is inherently linked to the slower growth rates that occur during nutrient limitation. Hardison et al.…”

Intraspecific Variability in the Toxin Production and Toxin Profiles of In Vitro Cultures of Gambierdiscus polynesiensis (Dinophyceae) from French Polynesia

“…Several studies have examined the toxin production patterns in relation to growth rates in various Gambierdiscus species such as G. polynesiensis, G. excentricus, G. australes, and G. carpenteri, and concluded to a higher toxin biosynthesis in strains/species with low reproductive rates [24,44,54,67,82]. These findings suggest a trade-off between investments of cellular resources in growth vs. the production of defensive compounds [24,54], a pattern also described in another closely related harmful algal species, Karenia brevis [83,84]. In any case, these observations on the potential effects of physiological factors (e.g., cell division rate and age of culture) on Gambierdiscus spp.…”

Photochemical release of sediment bound brevetoxin (PbTx-2) from resuspended sediments

“…brevis bloom (1.0 x 10 5 to > 1.0 x10 6 cells L -1 ) at the time of sediment collection in the vicinity of North Florida sample sites (NFx), Central Florida (CFx), and South Florida 1 (SF1) (Hardison et al, 2012;Hardison et al, 2013a;Hardison et al, 2013b;Hardison et al, 2014).…”