Mixotrophic microbes create carbon tipping points under warming

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 CO2 flux. 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 free Plain Language Summary for this article on the Journal blog.

Large protistan mixotrophs in the North Atlantic Continuous Plankton Recorder time series: associated environmental conditions and trends

“…A majority of current mixotroph predator-prey research focuses on the grazing impact of particular species or groups of plankton (Li et al, 2000;Seong et al, 2006;McKie-Krisberg et al, 2015;Millette et al, 2017), leaving the question of how the presence/absence of mixotrophs impacts the broader food-web unanswered. Theoretical modeling has begun to address how changes in the presence of mixotrophs alters the flow of carbon (Hartmann et al, 2013;Mitra et al, 2014;Ward and Follows, 2016;Wieczynski et al, 2023), but in situ measurements of mixotrophic activity are lacking. Our analysis emphasizes that there is seasonal and spatial variability in the proportion of the community composed of large (> 10 mm) mixotrophs, and that this variability is connected to basic environmental conditions.…”

“…Laboratory experiments have demonstrated more heterotrophic activity in mixotrophs with increasing temperature over shorter timeframes of hours, up to 20 h (Wilken et al, 2013), and longer adaptive timeframes of up to three years (Lepori-Bui et al, 2022). Further, in a mixotrophic food web model where protists could switch from phagotrophy to photoautotrophy and metabolic rates were temperature-dependent, environmental warming led to alternate stable states that were characterized as phototrophy-dominant carbon sinks vs. phagotrophy-dominant carbon sources; and warming always resulted in a phagotrophic carbon source system, even under stable nutrient conditions (Wieczynski et al, 2023). These results, alongside our findings, point to the theory that whole ecosystems may become net heterotrophic with increasing temperatures (Lopez-Urrutia et al, 2006;Wieczynski et al, 2023).…”

“…Further, in a mixotrophic food web model where protists could switch from phagotrophy to photoautotrophy and metabolic rates were temperature-dependent, environmental warming led to alternate stable states that were characterized as phototrophy-dominant carbon sinks vs. phagotrophy-dominant carbon sources; and warming always resulted in a phagotrophic carbon source system, even under stable nutrient conditions (Wieczynski et al, 2023). These results, alongside our findings, point to the theory that whole ecosystems may become net heterotrophic with increasing temperatures (Lopez-Urrutia et al, 2006;Wieczynski et al, 2023). This is an active and important current area of research.…”

Organic compounds drive growth in phytoplankton taxa from different functional groups

“…Mixotrophic phytoplankton can have a reduced chlorophyll content [ 7 , 15 , 33 ] and might therefore be underrepresented quantitatively with conventional measuring techniques that make use of pigment concentrations. Ultimately, recent studies show that integrating mixotrophy in climate change research is crucial for understanding carbon dynamics [ 34 , 35 ].…”

Temperature and CO2 interactively drive shifts in the compositional and functional structure of peatland protist communities

“…Predation by metazoans, in particular, plays a prominent role in peatland C cycling (Wyatt et al, 2021), and is likely to also impact microbial communities (Geisen et al, 2020;Rocca et al, 2022). Unicellular Eukaryotes, collectively known as protists, store two times more C globally than all animals combined (Bar-On et al, 2018;Bond-Lamberty & Thomson, 2010), contributing to C cycling through mixotrophic metabolism (Jassey et al, 2015;Wieczynski, Moeller, & Gibert, 2023), and also serve as one of the principal biological controls on microbial respiration and photosynthesis through predation and competition (Gao et al, 2019;Rocca et al, 2022;Thakur & Geisen, 2019). Protists also directly influence plant growth and health through their effects on the rhizosphere (Ceja-Navarro et al, 2021;Gao et al, 2019;Xiong et al, 2020) and phyllosphere (Bashir et al, 2022;Gómez-Pérez et al, 2022)-thus indirectly influencing plant growth through their effects on beneficial microorganisms (Geisen et al, 2020;Guo et al, 2021).…”