Protists and collembolans alter microbial community composition, C dynamics and soil aggregation in simplified consumer–prey systems

Abstract

Microbes play an essential role in soil functioning including biogeochemical cycling and soil aggregate formation. Yet, a major challenge is to link microbes to higher trophic levels and assess consequences for soil functioning. Here, we aimed to assess how microbial consumers modify microbial community composition (PLFA markers), as well as C dynamics (microbial C use, SOC concentration and CO$_2$ emission) and soil aggregation. We rebuilt two simplified soil consumer–prey systems: a bacterial-based system comprising amoebae (Acanthamoeba castellanii) feeding on a microbial community dominated by the free-living bacterium Pseudomonas fluorescens and a fungal-based system comprising collembolans (Heteromurus nitidus) grazing on a microbial community dominated by the saprotrophic fungus Chaetomium globosum. The amoeba A. castellanii did not affect microbial biomass and composition, but it enhanced the formation of soil aggregates and tended to reduce their stability. Presumably, the dominance of P. fluorescens, able to produce antibiotic toxins in response to the attack by A. castellanii, was the main cause of the unchanged microbial community composition, and the release of bacterial extracellular compounds, such as long-chained polymeric substances or proteases, in reaction to predation was responsible for the changes in soil aggregation as a side effect. In the fungal system, collembolans significantly modified microbial community composition via consumptive and non-consumptive effects including the transport of microbes on the body surface. As expected, fungal biomass promoted soil aggregation and was reduced in the presence of H. nitidus. Remarkably, we also found an unexpected contribution of changes in bacterial community composition to soil aggregation. In both the bacterial and fungal systems, bacterial and fungal communities mainly consumed C from soil organic matter (rather than the litter added). Increased fungal biomass was associated with an increased capture of C from added litter, and the presence of collembolans levelled off this effect. Neither amoebae nor collembolans altered SOC concentrations and CO$_2$ production. Overall, the results demonstrated that trophic interactions are important for achieving a mechanistic understanding of biological contributions to soil aggregation and may occur without major changes in C dynamics and with or without changes in the composition of the microbial community.