Mixotrophs in aquatic ecosystems : linking physiology to food web dynamics

Abstract

Mixotrophs combine traits from plants (autotrophs) and animals (heterotrophs. They can use sunlight for photosynthesis but also feed on other organisms. Understanding the intricate interaction and regulation of these autotrophic and heterotrophic processes within mixotrophs is essential for understanding their functional role in ecosystem processes, including their potential application as biological control agents against toxic cyanobacteria. This thesis combines lab experiments with mathematical models to study the ecophysiology and population dynamics of mixotrophs. The results shed new light on the applicability of several general ecological concepts to mixotrophs.

We confirmed one of the key predictions of the Metabolic Theory of Ecology that rates of heterotrophic processes increase more strongly with temperature than those of autotrophic processes. Consequently, mixotrophs become more heterotrophic with rising temperature. Nevertheless, the interaction between the two metabolic pathways can be complex. Structural changes in the photosynthetic machinery of Ochromonas danica during mixotrophic growth indicate that its photosynthesis mainly serves to provide energy rather than to fix inorganic carbon. Hence, mixotrophs might have a tendency towards photoheterotrophic growth.

Not only can the mixotrophic chrysophyte Ochromonas efficiently feed on harmful cyanobacteria and degrade the toxic microcystins, but its growth furthermore remained unaffected by the presence of the toxins in its prey. A dataset from Scandinavian lakes showed frequent co-occurrence of Microcystis and Ochromonas, with a relatively constant biomass of Ochromonas over a wide range of nutrient loads.

The mixotroph Ochromonas acts as intraguild predator of the cyanobacterium Microcystis as it both feeds on and competes with its autotrophic prey. We used these two species to test several of the key predictions of intraguild predation theory and could demonstrate that the combination of competition and predation indeed enables intraguild predators to suppress their prey more strongly than specialist predators can. However, contrary to theoretical predictions the intraguild prey Microcystis was favored relatively more by nutrient enrichment than its intraguild predator. These results can potentially be caused by several mechanisms, with intraspecific interference being a likely explanation during our chemostat experiments.

In conclusion, it is the balance between autotrophic and heterotrophic processes that defines the position of mixotrophs in food webs. This thesis demonstrates that the relative importance of alternative sources of carbon, energy and nutrients for mixotrophic growth depends on temperature, the chemical form of the required elements and the interaction of the different nutritional pathways on the subcellular level. Hence, all these factors can affect the grazing efficiency of mixotrophs and their competitive strength for inorganic resources. In turn, this will affect the population dynamics of mixotrophs and their prey and alter the functional role of mixotrophs in food webs.

Despite the remarkable ability of Ochromonas to graze on toxic cyanobacteria and to strongly suppress their abundance in controlled lab experiments, Ochromonas is unlikely to successfully control cyanobacterial growth in natural waters. Many of the common bloom-forming cyanobacteria, such as Microcystis, seem to be well protected against grazing by mixotrophic flagellates. Especially nutrient enrichment benefits the growth of Microcystis even in the presence of its intraguild predator.