Bacterial secondary metabolites serve as an important source of molecules for drug discovery. They also play an important function in mediating the interactions of microbial producers with their living environment and surrounding organisms. However, little is known about the genetic novelty, distribution, and community-level impacts of soil bacterial biosynthetic potential on a large geographic scale. Here, we constructed the first catalog of 11,149 biosynthetic gene clusters (BGCs) from agricultural soils across China and unearthed hidden biosynthetic potential for new natural product discovery from the not-yet-cultivated soil bacteria. Notably, we revealed soil pH as the strongest environmental driver of BGC biogeography and predicted that soil acidification and global climate change could damage the biosynthetic potential of the soil microbiome. The co-occurrence network of bacterial genomes revealed two BGC-rich species, i.e., Nocardia niigatensis from Actinobacteriota and PSRF01 from Acidobacteriota, as the module hub and connector, respectively, indicating their keystone positions in the soil microbial communities. We also uncovered a dominant role of BGC-inferred biotic interactions over environmental drivers in structuring the soil microbiome. Overall, this study achieved novel insights into the BGC landscape in agricultural soils of China, substantially expanding our understanding of the diversity and novelty of bacterial secondary metabolism and the potential role of secondary metabolites in microbiota assembly. IMPORTANCE Bacterial secondary metabolites not only serve as the foundation for numerous therapeutics (e.g., antibiotics and anticancer drugs), but they also play critical ecological roles in mediating microbial interactions (e.g., competition and communication). However, our knowledge of bacterial secondary metabolism is limited to only a small fraction of cultured strains, thus restricting our comprehensive understanding of their diversity, novelty, and potential ecological roles in soil ecosystems. Here, we used culture-independent metagenomics to explore biosynthetic potentials in agricultural soils of China. Our analyses revealed a high degree of genetic diversity and novelty within biosynthetic gene clusters in agricultural soil environments, offering valuable insights for biochemists seeking to synthesize novel bioactive products. Furthermore, we uncovered the pivotal role of BGC-rich species in microbial communities and the significant relationship between BGC richness and microbial phylogenetic turnover. This information emphasizes the importance of biosynthetic potential in the assembly of microbial communities.

Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partially- and fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions.