Reproducible Propagation of Species-Rich Soil Bacterial Communities Suggests Robust Underlying Deterministic Principles of Community Formation

Abstract

There is now a great awareness of the high diversity of most environmental (“free-living”) and host-associated microbiomes, but exactly how diverse microbial communities form and maintain is still highly debated. A variety of theories have been put forward, but testing them has been problematic because most studies have been based on synthetic communities that fail to accurately mimic the natural composition (i.e., the species used are typically not found together in the same environment), the diversity (usually too low to be representative), or the environmental system itself (using designs with single carbon sources or solely mixed liquid cultures).Microbiomes are typically characterized by high species diversity but it is poorly understood how such system-level complexity can be generated and propagated. Here, we used soil microcosms as a model to study development of bacterial communities as a function of their starting complexity and environmental boundary conditions. Despite inherent stochastic variation in manipulating species-rich communities, both laboratory-mixed medium complexity (21 soil bacterial isolates in equal proportions) and high-diversity natural top-soil communities followed highly reproducible succession paths, maintaining 16S rRNA gene amplicon signatures prominent for known soil communities in general. Development trajectories and compositional states were different for communities propagated in soil microcosms than in liquid suspension. Compositional states were maintained over multiple renewed growth cycles but could be diverged by short-term pollutant exposure. The different but robust trajectories demonstrated that deterministic taxa-inherent characteristics underlie reproducible development and self-organized complexity of soil microbiomes within their environmental boundary conditions. Our findings also have direct implications for potential strategies to achieve controlled restoration of desertified land. IMPORTANCE There is now a great awareness of the high diversity of most environmental (“free-living”) and host-associated microbiomes, but exactly how diverse microbial communities form and maintain is still highly debated. A variety of theories have been put forward, but testing them has been problematic because most studies have been based on synthetic communities that fail to accurately mimic the natural composition (i.e., the species used are typically not found together in the same environment), the diversity (usually too low to be representative), or the environmental system itself (using designs with single carbon sources or solely mixed liquid cultures). In this study, we show how species-diverse soil bacterial communities can reproducibly be generated, propagated, and maintained, either from individual isolates (21 soil bacterial strains) or from natural microbial mixtures washed from top-soil. The high replicate consistency we achieve both in terms of species compositions and developmental trajectories demonstrates the strong inherent deterministic factors driving community formation from their species composition. Generating complex soil microbiomes may provide ways for restoration of damaged soils that are prevalent on our planet.