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.

The harsh climatic conditions of deserts may lead to unique adaptations of microbes, which could serve as potential sources of new metabolites to cope with environmental stresses. However, the mechanisms governing the environmental adaptability and antimicrobial activity of desert Streptomyces remain inadequate, especially in extreme temperature differences, drought conditions, and strong radiation. Here, we isolated a Streptomyces strain from rocks in the Kumtagh Desert in Northwest China and tested its antibacterial activity, resistance to UV-C irradiation, and tolerance to hydrogen peroxide (H2O2). The whole-genome sequencing was carried out to study the mechanisms underlying physiological characteristics and ecological adaptation from a genomic perspective. This strain has a growth inhibitory effect against a variety of indicator bacteria, and the highest antibacterial activity recorded was against Bacillus cereus. Moreover, strain D23 can withstand UV-C irradiation up to 100 J/m(2) (D10 = 80 J/m(2)) and tolerate stress up to 70 mM H2O2. The genome prediction of strain D23 revealed the mechanisms associated with its adaptation to extreme environmental and stressful conditions. In total, 33 biosynthetic gene clusters (BGCs) were predicted based on anti-SMASH. Gene annotation found that S. huasconensis D23 contains several genes and proteins associated with the biosynthesis of factors required to cope with environmental stress of temperature, UV radiation, and osmotic pressure. The results of this study provide information about the genome and BGCs of the strain S. huasconensis D23. The experimental results combined with the genome sequencing data show that antimicrobial activity and stress resistance of S. huasconensis D23 was due to the rich and diverse secondary metabolite production capacity and the induction of stress-responsive genes. The environmental adaptability and antimicrobial activity information presented here will be valuable for subsequent work regarding the isolation of bioactive compounds and provide insight into the ecological adaptation mechanism of microbes to extreme desert environments.