COS 128-10
Individual-level functions and group-level byproducts: community context drives the scale of benefits in the toxic microalga, Prymnesium parvum
Many microbial taxa control their local environment. Microbial niche construction via secreted products may shape microbial communities in diverse environments. Many secreted products inhibit or kill competitors, ultimately allowing the producer lineage to monopolize an environment and the resources therein. However, it is not clear how such a strategy may invade a susceptible community from initial rarity, as the benefits of toxicity only accrue to toxic populations beyond a critical threshold density. Thus, co-occurring toxic and susceptible lineages should exhibit positive frequency-dependence, resulting in stable single-species equilibria in unstructured populations. Indeed, theory and experiments based on allelopathic bacteria have corroborated this expectation. These results imply an ecologically unstable strategy, and directly challenge classic explanations for the adaptive function of toxicity in bloom-forming microalgae, a diverse and important group of microbes. Unlike biofilm-forming bacteria, which may localize ecological benefits due to high local densities in structured environments, these microalgae typically exist as free-swimming unicells in planktonic populations. How, then, can the success of allelopathy in these environments be reconciled with established theoretical frameworks that predict an unstable ecological strategy? We use observations, co-culture experiments with toxic, predatory microalga Prymnesium parvum, and theoretical models in order to directly answer this question.
Results/Conclusions
We have isolated several species of microalgae from non-bloom and bloom communities in which P. parvum has become established. We formulated a flexible class of population dynamic models of two- and three-species communities, in order to determine the effects of cell-level benefits due to direct predation on the establishment of a toxic lineage, as well as the resulting community dynamics. A crucial distinction between these models is whether individual cells at low density may benefit from toxicity (e.g. through enhanced predation), or whether ecological benefits were restricted to improved access to nutrients through allelopathy.
We conducted experiments with P. parvum and three functionally unique classes of microalgae to empirically determine the best models for each two-species interaction. Each species interacted uniquely with toxic P. parvum. Armored desmids were resistant to P. parvum toxins, as well as consumption; armored diatoms were highly susceptible to toxicity, but resisted consumption; and naked chlorophytes could be quickly killed and consumed. Against diatoms, toxicity benefits all resistant lineages by reducing competition for nutrients, and desmids may act as true ‘cheaters’ under these conditions. However, introduction of unarmored competitors highlights a non-social, highly localized function of toxicity: the cell-level benefits of immobilizing and killing prey.