Changes in structure and assembly of a species-rich soil natural community with contrasting nutrient availability upon establishment of a plant-beneficial Pseudomonas in the wheat rhizosphere

Abstract

Abstract Background: Plant-beneficial bacterial inoculants are of great interest in agriculture as they have the potential to promote plant growth and health. However, the inoculation of the rhizosphere microbiome often results in a suboptimal or transient colonization, which is due to a variety of factors that influence the fate of the inoculant. To better understand the fate of plant-beneficial inoculants in complex rhizosphere microbiomes, composed by hundreds of genotypes and multifactorial selection mechanisms, controlled studies with high-complexity soil microbiomes are needed. Results: We analysed early compositional changes in a taxa-rich natural soil bacterial community, both in exponential nutrient-rich or stationary nutrient-limited growth conditions (i.e., growing and stable communities, respectively), upon inoculation by the plant-beneficial bacterium Pseudomonas protegens in a bulk soil or a wheat rhizosphere environment. P. protegens successfully established in all conditions tested, being more abundant in the rhizosphere of the stable community. Nutrient availability was a major factor driving microbiome composition and structure as well as the underlying assembly processes. While access to nutrients resulted in communities being mainly assembled by homogeneous selection, stochastic processes dominated in the nutrient-deprived conditions. We also observed an increased rhizosphere selection effect on nutrient-limited conditions, resulting in higher numbers of amplicon sequence variants (ASVs) whose relative abundance was enriched. The inoculation with P. protegens produced discrete changes, some of which involved other Pseudomonas. Direct competition between Pseudomonas strains partially failed to replicate differences observed in the microbiome and pointed to a more complex interaction network. Conclusions: The results obtained in this study show that nutrient availability is a major driving force of microbiome composition, structure, and diversity both in the bulk soil and the wheat rhizosphere and determines the assembly processes governing early microbiome development. The successful establishment of the inoculant was facilitated by the wheat rhizosphere and produced discrete changes among other members of the microbiome. Direct competition between Pseudomonas strains only partially explained microbiome changes and revealed that indirect interactions or spatial distribution in the rhizosphere or soil interface could be crucial for the survival of certain bacteria.