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Abstract Mixotrophs are ubiquitous and integral to microbial food webs, but their impacts on the dynamics and functioning of broader ecosystems are largely unresolved.Here, we show that mixotrophy produces a unique type of food web module that exhibits unusual ecological dynamics, with surprising consequences for carbon flux under warming. We develop a generalizable model of a mixotrophic food web module that incorporates dynamic switching between phototrophy and phagotrophy to assess ecological dynamics and total system CO₂flux.We find that warming switches mixotrophic systems between alternative stable carbon states—including a phototrophy‐dominant carbon sink state, a phagotrophy‐dominant carbon source state and cycling between these two. Moreover, warming always shifts this mixotrophic system from a carbon sink state to a carbon source state, but a coordinated increase in nutrients can erase early warning signals of this transition and expand hysteresis.This suggests that mixotrophs can generate critical carbon tipping points under warming that will be more abrupt and less reversible when combined with increased nutrient levels, having widespread implications for ecosystem functioning in the face of rapid global change. Read the freePlain Language Summaryfor this article on the Journal blog. 

Abstract Rising ocean temperatures affect marine microbial ecosystems directly, since metabolic rates (e.g., photosynthesis, respiration) are temperature‐dependent, but temperature also has indirect effects mediated through changes to the physical environment. Empirical observations of the long‐term trends in biomass and productivity measure the integrated response of these two kinds of effects, making the independent components difficult to disentangle. We used a combination of modeling approaches to isolate the direct effects of rising temperatures on microbial metabolism and explored the consequences for food web dynamics and global biogeochemistry. We evaluated the effects of temperature sensitivity in two cases: first, assuming that all metabolic processes have the same temperature sensitivity, or, alternatively, that heterotrophic processes have higher temperature sensitivity than autotrophic processes. Microbial ecosystems at higher temperatures are characterized by increased productivity but decreased biomass stocks as a result of transient, high export events that reduce nutrient availability in the surface ocean. Trophic dynamics also mediate community structure shifts resulting in increased heterotroph to autotroph ratios at higher temperatures. These ecosystem thermal responses are magnified when the temperature sensitivity of heterotrophs is higher than that of autotrophs. These results provide important context for understanding the combined food web response to direct and indirect temperature effects and inform the construction and interpretation of Earth systems models used in climate projections. 

Abstract Mixotrophs, organisms that combine photosynthesis and heterotrophy to gain energy, play an important role in global biogeochemical cycles. Metabolic theory predicts that mixotrophs will become more heterotrophic with rising temperatures, potentially creating a positive feedback loop that accelerates carbon dioxide accumulation in the atmosphere. Studies testing this theory have focused on phenotypically plastic (short‐term, non‐evolutionary) thermal responses of mixotrophs. However, as small organisms with short generation times and large population sizes, mixotrophs may rapidly evolve in response to climate change. Here, we present data from a 3‐year experiment quantifying the evolutionary response of two mixotrophic nanoflagellates to temperature. We found evidence for adaptive evolution (increased growth rates in evolved relative to acclimated lineages) in the obligately phototrophic strain, but not in the facultative phototroph. All lineages showed trends of increased carbon use efficiency, flattening of thermal reaction norms, and a return to homeostatic gene expression. Generally, mixotrophs evolved reduced photosynthesis and higher grazing with increased temperatures, suggesting that evolution may act to exacerbate mixotrophs' effects on global carbon cycling. 

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. 

Abstract Acquired phototrophs, organisms that obtain their photosynthetic abilities by hosting endosymbionts or stealing plastids from their prey, are omnipresent in aquatic ecosystems. This acquisition of photosynthetic metabolism allows for niche expansion, and can therefore influence competition outcomes by alleviating competition for shared resources. Here, we test how acquired metabolism alters competitive outcomes by manipulating light availability to control the energetic contribution of photosynthesis to acquired phototrophs. Using freshwater protists that compete for bacterial prey, we demonstrate light‐dependent competition outcomes of acquired phototrophs ( Paramecium bursaria ) and strict heterotrophs ( Colpidium sp.) in laboratory model experiments. We then synthesize these findings using a series of mathematical models, and show that explicitly accounting for resource competition improves model fits. Both empirical and mathematical models predict that the acquired phototroph should increase in competitive dominance with increasing light availability. Our results highlight the importance of acquired metabolism to community dynamics, highlighting the need for more empirical and theoretical studies of this mechanism for niche expansion.