Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures

Abstract

Background Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to the ecosystem level. While mixotrophic phytoplankton, organisms that combine photosynthesis and heterotrophy to meet their energetic and nutritional needs, are expected to become more heterotrophic with warmer temperatures due to heterotrophy increasing at a faster rate than photosynthesis, it is unclear how evolution will influence how these organisms respond to warmer temperatures. In this study, we used adaptive dynamics to model the consequences of temperature-mediated increases in metabolic rates for the evolution of mixotrophic phytoplankton, focusing specifically on phagotrophic mixotrophs. Results We find that mixotrophs tend to evolve to become more reliant on phagotrophy as temperatures rise, leading to reduced prey abundance through higher grazing rates. However, if prey abundance becomes too low, evolution favors greater reliance on photosynthesis. These responses depend upon the trade-off that mixotrophs experience between investing in photosynthesis and phagotrophy. Mixotrophs with a convex trade-off maintain mixotrophy over the greatest range of temperatures; evolution in these “generalist” mixotrophs was found to exacerbate carbon cycle impacts, with evolving mixotrophs exhibiting increased sensitivity to rising temperature. Conclusions Our results show that mixotrophs may respond more strongly to climate change than predicted by phenotypic plasticity alone due to evolutionary shifts in metabolic investment. However, the type of metabolic trade-off experienced by mixotrophs as well as ecological feedback on prey abundance may ultimately limit the extent of evolutionary change along the heterotrophy-phototrophy spectrum.

Transcriptomic insights into the shift of trophic strategies in mixotrophic dinoflagellate Lepidodinium in the warming ocean

“…We supposed that the prey abundance was too low to support the cell growth in this condition, which reduces the favorability of grazing and phagotrophic investment. This finding was consistent with a recent modeling study which predicted that mixotrophs tend to evolve to become more reliant on phagotrophy at higher temperatures, but if prey abundance becomes too low, evolution favors greater reliance on photosynthesis [ 75 ]. When Chl- a concentration was >0.3 mg.m −3 , only one photosynthesis gene significantly positively correlated to temperature ( Fig.…”

Recommendations for advancing mixoplankton research through empirical-model integration

“…These models simulate evolution as a series of small mutations in an organism's (functional) trait(s) and are used to identify evolutionarily stable strategies (ESSs) that are robust to invasion by slightly different strategies (Diekmann, 2003). Such models have been used to identify environmental conditions under which mixotrophs should specialize (Troost et al, 2005b(Troost et al, , 2005a, to evaluate a mixotroph's optimal balance between phagotrophy and phototrophy as a function of environmental temperature (Gonzalez et al, 2022), and to understand the adaptiveness of kleptoplasty (Brown et al, 2023). These theoretical predictions can be tested with new data on the distribution (and plasticity) of mixotrophs in nature, and better constrained by data on the phylogeny of mixotrophs and their traits.…”