The cost of toxin production in phytoplankton: the case of PST producing dinoflagellates

Abstract

Many species of phytoplankton produce toxins that may provide protection from grazing. In that case one would expect toxin production to be costly; else all species would evolve toxicity. However, experiments have consistently failed to show any costs. Here, we show that costs of toxin production are environment dependent but can be high. We develop a fitness optimization model to estimate rate, costs, and benefits of toxin production, using PST (paralytic shellfish toxin) producing dinoflagellates as an example. Costs include energy and material (nitrogen) costs estimated from well-established biochemistry of PSTs, and benefits are estimated from relationship between toxin content and grazing mortality. The model reproduces all known features of PST production: inducibility in the presence of grazer cues, low toxicity of nitrogen-starved cells, but high toxicity of P-limited and light-limited cells. The model predicts negligible reduction in cell division rate in nitrogen replete cells, consistent with observations, but >20% reduction when nitrogen is limiting and abundance of grazers high. Such situation is characteristic of coastal and oceanic waters during summer when blooms of toxic algae typically develop. The investment in defense is warranted, since the net growth rate is always higher in defended than in undefended cells.

Competition–defense tradeoff increases the diversity of microbial plankton communities and dampens trophic cascades

“…Such blooms are usually observed under summer conditions of nutrient limitation and concurrent with the stabilization of the water column (Hakanen et al 2012, Gettings et al 2014, Sourisseau et al 2017) and the highest seasonal abundance of copepod grazers (Kiørboe and Nielsen 1994). These are the conditions that stimulate the induction of costly defense in dinoflagellates (Chakraborty et al 2018). While this is consistent with the predictions of our model (i.e.…”

“…However, toxin production is inducible, i.e. produced in much higher quantities in the presence of grazer cues (Selander et al 2006), strongly suggesting that toxin production is indeed costly, but the costs may only materialize when resources are limiting (Chakraborty et al 2018).…”

“…1b) depends on the defense mechanism as well as on environmental conditions (Loeuille and Loreau 2004). For example, stealth behavior reduces the resource affinity (Kiørboe et al 2014) and production of defense toxins may reduce the resources available for growth in protists (Brandenburg et al 2018), but mainly when resources are limiting (Chakraborty et al 2018).…”

On biological evolution and environmental solutions

“…For example, some lineages entirely lack the genes for toxin production (Brandenburg et al, 2018;Briand et al, 2009). The evolutionary dynamics of different toxic/non-toxic genotypes during algal blooms is likely driven by physiological trade-offs between costs of toxin production and resource uptake for growth (Brandenburg et al, 2018;Cadier et al, 2019;Chakraborty et al, 2019;Kiørboe and Andersen, 2019). Such defense-growth trade-offs are likely important for the emergence of harmful algal blooms (Burford et al, 2019;Jankowiak et al, 2019;Kim et al, 2010;Li et al, 2012), but the selective factors that favor toxic variants in bloom forming algae are not fully understood.…”

Nutrient affinity, half-saturation constants and the cost of toxin production in dinoflagellates

“…The difficulty of quantifying trade-offs applies to several other defence mechanisms (Pan ci c & Kiørboe 2018). One reason may be that costs are significant only under resource limitation (Meaden et al 2015;Zhu et al 2016;Chakraborty et al 2018). The experiments of Brandenburg et al and those of others looking for costs of toxin production in dinoflagellates have not explored this possibility.…”