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

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 ar...

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Bibliographic Details
Published in:The ISME Journal 2019-01, Vol.13 (1), p.64-75
Main Authors: Chakraborty, Subhendu, Pančić, Marina, Andersen, Ken H, Kiørboe, Thomas
Format: Article
Language:English
Subjects:
Algae
Animals
Biological evolution
Cell division
Coastal waters
Costs
Dinoflagellata
Dinoflagellates
Dinoflagellida - metabolism
Energy costs
Energy Metabolism - physiology
Fitness
Grazing
Growth rate
Marine Toxins - metabolism
Microorganisms
Models, Biological
Nitrogen
Nitrogen - metabolism
Optimization
Phytoplankton
Phytoplankton - classification
Phytoplankton - metabolism
Reduction
Shellfish
Toxicity
Toxins
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Summary: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.
ISSN:1751-7362
1751-7370
DOI:10.1038/s41396-018-0250-6