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Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity.

ABSTRACT: Numerous therapeutically relevant small molecules have been identified from the screening of natural products (NPs) produced by environmental bacteria. These discovery efforts have principally focused on culturing bacteria from natural environments rich in biodiversity. We sought to assess the biosynthetic capacity of urban soil environments using a phylogenetic analysis of conserved NP biosynthetic genes amplified directly from DNA isolated from New York City park soils. By sequencing genes involved in the biosynthesis of nonribosomal peptides and polyketides, we found that urban park soil microbiomes are both rich in biosynthetic diversity and distinct from nonurban samples in their biosynthetic gene composition. A comparison of sequences derived from New York City parks to genes involved in the biosynthesis of biomedically important NPs produced by bacteria originally collected from natural environments around the world suggests that bacteria producing these same families of clinically important antibiotics, antifungals, and anticancer agents are actually present in the soils of New York City. The identification of new bacterial NPs often centers on the systematic exploration of bacteria present in natural environments. Here, we find that the soil microbiomes found in large cities likely hold similar promise as rich unexplored sources of clinically relevant NPs.

SUBMITTER: Charlop-Powers Z

PROVIDER: S-EPMC5187742 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity.

Charlop-Powers Zachary Z Pregitzer Clara C CC Lemetre Christophe C Ternei Melinda A MA Maniko Jeffrey J Hover Bradley M BM Calle Paula Y PY McGuire Krista L KL Garbarino Jeanne J Forgione Helen M HM Charlop-Powers Sarah S Brady Sean F SF

Proceedings of the National Academy of Sciences of the United States of America 20161128 51

Numerous therapeutically relevant small molecules have been identified from the screening of natural products (NPs) produced by environmental bacteria. These discovery efforts have principally focused on culturing bacteria from natural environments rich in biodiversity. We sought to assess the biosynthetic capacity of urban soil environments using a phylogenetic analysis of conserved NP biosynthetic genes amplified directly from DNA isolated from New York City park soils. By sequencing genes inv ...[more]

PMID: 27911822

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Project description:BackgroundAntibiotic resistance is a growing problem that can be ameliorated by the discovery of novel drug candidates. Bacterial associates are often the source of pharmaceutically active natural products isolated from marine invertebrates, and thus, important targets for drug discovery. While the microbiomes of many marine organisms have been extensively studied, microbial communities from chemically-rich nudibranchs, marine invertebrates that often possess chemical defences, are relatively unknown.MethodsWe applied both culture-dependent and independent approaches to better understand the biochemical potential of microbial communities associated with nudibranchs. Gram-positive microorganisms isolated from nudibranchs collected in the Red Sea were screened for antibacterial and antitumor activity. To assess their biochemical potential, the isolates were screened for the presence of natural product biosynthetic gene clusters, including polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS) genes, using PCR. The microbiomes of the nudibranchs were investigated by high-throughput sequencing of 16S rRNA amplicons.ResultsIn screens against five model microorganisms, 51% of extracts displayed antimicrobial activity against more than one organism, and 19% exhibited antitumor activity against Ehrlich's ascites carcinoma. Sixty-four percent of isolates contained PKS and NRPS genes, suggesting their genomes contain gene clusters for natural product biosynthesis. Thirty-five percent were positive for more than one class of biosynthetic gene. These strains were identified as belonging to the Firmicutes and Actinobacteria phyla via 16S rRNA gene sequencing. In addition, 16S rRNA community amplicon sequencing revealed all bacterial isolates were present in the uncultured host-associated microbiome, although they were a very small percentage of the total community. Taken together, these results indicate that bacteria associated with marine nudibranchs are potentially a rich source of bioactive compounds and natural product biosynthetic genes.

Project description: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.IMPORTANCEBacterial 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.

Project description:BackgroundThe rapid expansion of urbanization leads to significant losses of soil ecological functions. Microbes directly participate in key soil processes and play crucial roles in maintaining soil functions. However, we still have a limited understanding of underlying mechanisms shaping microbial communities and the interactions among microbial taxa in park soils.MethodsIn this study, the community variations of bacteria and fungi in urban and suburban park soils were investigated in Shanghai, China. Real-time PCR and high-throughput Illumina sequencing were used to examine the microbial abundance and community composition, respectively.ResultsThe results showed that soil molecular biomass and fungal abundance in urban park soils were significantly higher than those in suburban park soils, while no significant difference was observed in the bacterial abundance between urban and suburban park soils. The alpha diversity of soil microbes in urban and suburban park soils was similar to each other, except for Chao1 index of fungal communities. The results of similarity analysis (ANOSIM) revealed remarkable differences in the composition of bacterial and fungal communities between urban and suburban park soils. Specifically, park soils in urban areas were enriched with the phyla Methylomirabilota and Verrucomicrobiota, while the relative abundance of Gemmatimonadota was higher in suburban park soils. Moreover, the fungal class Eurotiomycetes was also enriched in urban park soils. Compared with suburban park soils, nodes and average paths of the bacterial and fungal networks were higher in urban park soils, but the number of module hubs and connectors of the bacterial networks and negative interactions among bacterial taxa were lower. Compared with suburban park soils, Acidobacteriota bacterium and Mortierellomycota fungus played more important roles in the ecological networks of urban park soils. Soil available zinc (Zn), available nitrogen (N), pH, and total potassium (K) significantly affected fungal community composition in park soils in Shanghai. Soil available Zn was also the most important factor affecting the bacterial community composition in this study.ConclusionThere were significant differences in the soil molecular biomass, fungal abundance, and the community composition and co-occurrence relations of both soil bacterial and fungal communities between urban and suburban park soils. Soil available Zn played an important part in shaping the structures of both the bacterial and fungal communities in park soils in Shanghai.

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Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity.

Publications

Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity.

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