Body size mediates the functional potential of soil organisms by diversity and community assembly across soil aggregates.

Body size is an important life-history trait that affects organism niche occupancy and ecological interactions. However, it is still unclear to what extent the assembly process of organisms with different body sizes affects soil biogeochemical cycling processes at the aggregate level. Here, we examined the diversity and community assembly of soil microorganisms (bacteria, fungi, and protists) and microfauna (nematodes) with varying body sizes. The microbial functional potential associated with carbon, nitrogen, phosphorus, and sulfur metabolism within three soil aggregate sizes (large macroaggregates, > 2 mm; small macroaggregates, 0.25-2 mm; and microaggregates, < 0.25 mm) were determined by metagenomics. We found that the smallest microbes (bacteria) had higher α-diversity and lower ß-diversity and were mostly structured by stochastic processes, while all larger organisms (fungi, protists, and nematodes) had lower α-diversity and were relatively more influenced by deterministic processes. Structural equation modeling indicated that the microbial functional potential associated with carbon, nitrogen, phosphorus, and sulfur metabolism was mainly influenced by the bacterial and protist diversity in microaggregates. In contrast, the microbial functional potential was primarily mediated by the assembly processes of four organism groups, especially the nematode community in macroaggregates. This study reveals the important roles of soil organisms with different body sizes in the functional potential related to nutrient cycling, and provides new insights into the ecological processes structuring the diversity and community assembly of organisms of different body sizes at the soil aggregate level, with implications for soil nutrient cycling dynamics.

Nematode Predation and Competitive Interactions Affect Microbe-Mediated Phosphorus Dynamics.

Nematode predation plays an essential role in determining changes in the rhizosphere microbiome. These changes affect the local nutrient balance and cycling of essential nutrients by selectively structuring interactions across functional taxa in the system. Currently, it is largely unknown to what extent nematode predation induces shifts in the microbiome associated with different rates of soil phosphorous (P) mineralization. Here, we performed an 7-year field experiment to investigate the importance of nematode predation influencing P availability and cycling. These were tracked via the changes in the alkaline phosphomonoesterase (ALP)-producing bacterial community and ALP activity in the rhizosphere of rapeseed. Here, we found that the nematode addition led to high predation pressure and thereby caused shifts in the abundance and composition of the ALP-producing bacterial community. Further analyses based on cooccurrence networks and metabolomics consistently showed that nematode addition induced competitive interactions between potentially keystone ALP-producing bacteria and other members within the community. Structural equation modeling revealed that the outcome of this competition induced by stronger predation pressure of nematodes was significantly associated with higher diversity of ALP-producing bacteria, thereby enhancing ALP activity and P availability. Taken together, our results provide evidence for the importance of predator-prey and competitive interactions in soil biology and their direct influences on nutrient cycling dynamics. IMPORTANCE Nematode predation plays an essential role in determining the rhizosphere microbiome. In doing so, predation dynamically affects the soil nutrient cycling, for instance, by shifting the availability of phosphorus (P) for plant uptake. However, the role of nematode predation inducing selective changes in the microbiome and affecting rates of P mineralization remains still largely unknown. Here, we used a field site treated with different fertilizers to investigate the importance of nematode predation influencing P availability and plant productivity, via changes in bacterial taxa producing alkaline phosphomonoesterases (ALP) and ALP activity in the rhizosphere of rapeseed. We integrated field and laboratory experiments to show that nematode predation induces bacterial keystone taxa to compete with the connected members and results in the modulation of ALP-producing bacterial populations and ALP activity in the rhizosphere. Taken together, our study provides novel insights into microbially mediated mechanisms of competitive interaction induced by nematode predation in enhancing P availability in the plant rhizosphere.

Rhizosphere protists are key determinants of plant health.

BACKGROUND: Plant health is intimately influenced by the rhizosphere microbiome, a complex assembly of organisms that changes markedly across plant growth. However, most rhizosphere microbiome research has focused on fractions of this microbiome, particularly bacteria and fungi. It remains unknown how other microbial components, especially key microbiome predators-protists-are linked to plant health. Here, we investigated the holistic rhizosphere microbiome including bacteria, microbial eukaryotes (fungi and protists), as well as functional microbial metabolism genes. We investigated these communities and functional genes throughout the growth of tomato plants that either developed disease symptoms or remained healthy under field conditions. RESULTS: We found that pathogen dynamics across plant growth is best predicted by protists. More specifically, communities of microbial-feeding phagotrophic protists differed between later healthy and diseased plants at plant establishment. The relative abundance of these phagotrophs negatively correlated with pathogen abundance across plant growth, suggesting that predator-prey interactions influence pathogen performance. Furthermore, phagotrophic protists likely shifted bacterial functioning by enhancing pathogen-suppressing secondary metabolite genes involved in mitigating pathogen success. CONCLUSIONS: We illustrate the importance of protists as top-down controllers of microbiome functioning linked to plant health. We propose that a holistic microbiome perspective, including bacteria and protists, provides the optimal next step in predicting plant performance. Video Abstract.