An official website of the United States government
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.
more »
« less
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 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.
more »
« less
- Award ID(s):
- 1851194
- PAR ID:
- 10420787
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Functional Ecology
- Volume:
- 37
- Issue:
- 7
- ISSN:
- 0269-8463
- Format(s):
- Medium: X Size: p. 1774-1786
- Size(s):
- p. 1774-1786
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Mixotrophic protists combine photosynthesis and phagotrophy to obtain energy and nutrients. Because mixotrophs can act as either primary producers or consumers, they have a complex role in marine food webs and biogeochemical cycles. Many mixotrophs are also phenotypically plastic and can adjust their metabolic investments in response to resource availability. Thus, a single species's ecological role may vary with environmental conditions. Here, we quantified how light and food availability impacted the growth rates, energy acquisition rates, and metabolic investment strategies of eight strains of the mixotrophic chrysophyte,Ochromonas. All eightOchromonasstrains photoacclimated by decreasing chlorophyll content as light intensity increased. Some strains were obligate phototrophs that required light for growth, while other strains showed stronger metabolic responses to prey availability. When prey availability was high, all eight strains exhibited accelerated growth rates and decreased their investments in both photosynthesis and phagotrophy. Photosynthesis and phagotrophy generally produced additive benefits: In low‐prey environments,Ochromonasgrowth rates increased to maximum, light‐saturated rates with increasing light but increased further with the addition of abundant bacterial prey. The additive benefits observed between photosynthesis and phagotrophy inOchromonassuggest that the two metabolic modes provide nonsubstitutable resources, which may explain why a tradeoff between phagotrophic and phototrophic investments emerged in some but not all strains.more » « less
-
Abstract Biogeochemical cycling has often been characterized by physical and microbial processes, yet animals can be essential mediators of energy and nutrients in ecosystems. Excretion by aggregated animals can be an important local source of inorganic nutrients in green food webs; however, whether animals are a source of dissolved energy that can support brown food webs is understudied.We tested whether animal aggregations are a substantial flux of bioavailable dissolved organic matter (DOM) by studying spatially stable, biogeochemical hotspots formed by filter‐feeding freshwater mussels. We used parallel‐factor analysis to quantify DOM fluorescent components composition of mussel excretion and expected digestive breakdown of particulate food sources would lead to excretion of labile DOM. Next, we combined measured excretion rates of DOM, ammonium (, N) and phosphorous (SRP; P) for 22 species with biomass estimates for 14 aggregations to quantify contributions of DOM, N and P to local availability. Because mussels occupy distinct stoichiometric niches, we anticipated that differences in species biomass and assemblage structure would elicit different flux and stoichiometries of aggregate excretion.Aggregate dissolved organic carbon (DOC) excretion was minor (1%–11%) compared to N (12%–2,860%) and P (1%–97%), yet generalities across assemblages emerged regarding organic matter transformation by mussels towards labile protein‐like compounds compared to abundant aromatic, humic compounds in ambient water.Aggregate excretion of labile DOM was a substantial pool of bioavailable energy, contributing 2%–114% of local labile DOM. Spatial differences in assemblage structure led to strong differences in aggregate flux and stoichiometry driven by biomass and stoichiometric trait expression of species with contrasting dominance patterns.Under the nutrient conditions of our study (high C:nutrient), biogeochemical hotspots associated with low‐trophic position animal biomass may indirectly control energy flow to the brown food web by shifting C:nutrient stoichiometry available to microbes or directly by increasing the flux of microbially available DOM. Collectively, our results highlight a potentially substantial flux of labile energy and nutrients to microbial communities through the transformation of ingested organic matter by aggregations of animals and emphasize that shared functional trait classification may not translate into shared ecological function. A freePlain Language Summarycan be found within the Supporting Information of this article.more » « less
-
Abstract Small eukaryotic phytoplankton are major contributors to global primary production and marine biogeochemical cycles. Many taxa are thought to be mixotrophic, but quantitative studies of phagotrophy exist for very few. In addition, little is known about consumers of Prochlorococcus, the abundant cyanobacterium at the base of oligotrophic ocean food webs. Here we describe thirty-nine new phytoplankton isolates from the North Pacific Subtropical Gyre (Station ALOHA), all flagellates ~2–5 µm diameter, and we quantify their ability to graze Prochlorococcus. The mixotrophs are from diverse classes (dictyochophytes, haptophytes, chrysophytes, bolidophytes, a dinoflagellate, and a chlorarachniophyte), many from previously uncultured clades. Grazing ability varied substantially, with specific clearance rate (volume cleared per body volume) varying over ten-fold across isolates and six-fold across genera. Slower grazers tended to create more biovolume per prey biovolume consumed. Using qPCR we found that the haptophyte Chrysochromulina was most abundant among the isolated mixotrophs at Station ALOHA, with 76–250 cells mL−1 across depths in the upper euphotic zone (5–100 m). Our results show that within a single ecosystem the phototrophs that ingest bacteria come from many branches of the eukaryotic tree, and are functionally diverse, indicating a broad range of strategies along the spectrum from phototrophy to phagotrophy.more » « less
-
Abstract In sunlit waters, significant predation is performed by unicellular, phagotrophic mixotrophs, that is, predators that also possess plastids. The success of a mixotrophic lifestyle will depend in part on how well mixotrophs acquire prey relative to specialized heterotrophs. Likewise, consequences of mixotrophy for productivity and element cycling will depend on the rate and efficiency at which mixotrophs consume prey biomass relative to heterotrophs. However, trait differences between mixotrophs and heterotrophs are not well characterized. In addition, cell size of mixotrophs varies widely, and constitutive mixotrophs include small flagellates deriving from diverse taxa, while larger species are primarily dinoflagellates. To determine whether similar constraints apply to phagotrophs across this broad range of size and taxa, we compiled 83 measurements of flagellate functional responses and compared maximum clearance rates (Cmax) and maximum ingestion rates (Imax) between trophic modes. We found that the average mixotroph has a 3.7‐fold lowerCmaxand 7.8‐fold lowerImaxthan the average heterotroph, after controlling for cell size. The smaller penalty forCmaxsuggests that relative fitness of mixotrophs will be enhanced under dilute prey concentrations that are common in pelagic ecosystems. We also find that growth efficiency is greater for mixotrophs and for flagellates with lowerCmax, indicating a spectrum of trophic strategies that may be driven by phototrophy vs. phagotrophy allocation as well as fast vs. slow metabolic variation. Allometric scaling shows thatImaxis constrained by a common relationship among dinoflagellates and other taxa, but dinoflagellates achieve a greater volume‐specificCmax. These results should aid in interpreting protistan communities and modeling mixotrophy.more » « less
