Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potential
Background Streptomyces is a highly diverse genus known for the production of secondary or specialized metabolites with a wide range of applications in the medical and agricultural industries. Several thousand complete or nearly complete Streptomyces genome sequences are now available, affording the...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2025-01-01
|
| Series: | Genome Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13059-024-03471-9 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832594712063639552 |
|---|---|
| author | Omkar S. Mohite Tue S. Jørgensen Thomas J. Booth Pep Charusanti Patrick V. Phaneuf Tilmann Weber Bernhard O. Palsson |
| author_facet | Omkar S. Mohite Tue S. Jørgensen Thomas J. Booth Pep Charusanti Patrick V. Phaneuf Tilmann Weber Bernhard O. Palsson |
| author_sort | Omkar S. Mohite |
| collection | DOAJ |
| description | Background Streptomyces is a highly diverse genus known for the production of secondary or specialized metabolites with a wide range of applications in the medical and agricultural industries. Several thousand complete or nearly complete Streptomyces genome sequences are now available, affording the opportunity to deeply investigate the biosynthetic potential within these organisms and to advance natural product discovery initiatives. Results We perform pangenome analysis on 2371 Streptomyces genomes, including approximately 1200 complete assemblies. Employing a data-driven approach based on genome similarities, the Streptomyces genus was classified into 7 primary and 42 secondary Mash-clusters, forming the basis for comprehensive pangenome mining. A refined workflow for grouping biosynthetic gene clusters (BGCs) redefines their diversity across different Mash-clusters. This workflow also reassigns 2729 known BGC families to only 440 families, a reduction caused by inaccuracies in BGC boundary detections. When the genomic location of BGCs is included in the analysis, a conserved genomic structure, or synteny, among BGCs becomes apparent within species and Mash-clusters. This synteny suggests that vertical inheritance is a major factor in the diversification of BGCs. Conclusions Our analysis of a genomic dataset at a scale of thousands of genomes refines predictions of BGC diversity using Mash-clusters as a basis for pangenome analysis. The observed conservation in the order of BGCs’ genomic locations shows that the BGCs are vertically inherited. The presented workflow and the in-depth analysis pave the way for large-scale pangenome investigations and enhance our understanding of the biosynthetic potential of the Streptomyces genus. |
| format | Article |
| id | doaj-art-a418ca0c031640c38170a410c743b197 |
| institution | Kabale University |
| issn | 1474-760X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj-art-a418ca0c031640c38170a410c743b1972025-01-19T12:25:37ZengBMCGenome Biology1474-760X2025-01-0126112010.1186/s13059-024-03471-9Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potentialOmkar S. Mohite0Tue S. Jørgensen1Thomas J. Booth2Pep Charusanti3Patrick V. Phaneuf4Tilmann Weber5Bernhard O. Palsson6The Novo Nordisk Foundation Center for Biosustainability, Technical University of DenmarkThe Novo Nordisk Foundation Center for Biosustainability, Technical University of DenmarkThe Novo Nordisk Foundation Center for Biosustainability, Technical University of DenmarkThe Novo Nordisk Foundation Center for Biosustainability, Technical University of DenmarkThe Novo Nordisk Foundation Center for Biosustainability, Technical University of DenmarkThe Novo Nordisk Foundation Center for Biosustainability, Technical University of DenmarkThe Novo Nordisk Foundation Center for Biosustainability, Technical University of DenmarkBackground Streptomyces is a highly diverse genus known for the production of secondary or specialized metabolites with a wide range of applications in the medical and agricultural industries. Several thousand complete or nearly complete Streptomyces genome sequences are now available, affording the opportunity to deeply investigate the biosynthetic potential within these organisms and to advance natural product discovery initiatives. Results We perform pangenome analysis on 2371 Streptomyces genomes, including approximately 1200 complete assemblies. Employing a data-driven approach based on genome similarities, the Streptomyces genus was classified into 7 primary and 42 secondary Mash-clusters, forming the basis for comprehensive pangenome mining. A refined workflow for grouping biosynthetic gene clusters (BGCs) redefines their diversity across different Mash-clusters. This workflow also reassigns 2729 known BGC families to only 440 families, a reduction caused by inaccuracies in BGC boundary detections. When the genomic location of BGCs is included in the analysis, a conserved genomic structure, or synteny, among BGCs becomes apparent within species and Mash-clusters. This synteny suggests that vertical inheritance is a major factor in the diversification of BGCs. Conclusions Our analysis of a genomic dataset at a scale of thousands of genomes refines predictions of BGC diversity using Mash-clusters as a basis for pangenome analysis. The observed conservation in the order of BGCs’ genomic locations shows that the BGCs are vertically inherited. The presented workflow and the in-depth analysis pave the way for large-scale pangenome investigations and enhance our understanding of the biosynthetic potential of the Streptomyces genus.https://doi.org/10.1186/s13059-024-03471-9Pangenome analysisStreptomycesGenome miningBiosynthetic Gene ClustersPhylogenetic analysisMetabolism |
| spellingShingle | Omkar S. Mohite Tue S. Jørgensen Thomas J. Booth Pep Charusanti Patrick V. Phaneuf Tilmann Weber Bernhard O. Palsson Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potential Genome Biology Pangenome analysis Streptomyces Genome mining Biosynthetic Gene Clusters Phylogenetic analysis Metabolism |
| title | Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potential |
| title_full | Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potential |
| title_fullStr | Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potential |
| title_full_unstemmed | Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potential |
| title_short | Pangenome mining of the Streptomyces genus redefines species’ biosynthetic potential |
| title_sort | pangenome mining of the streptomyces genus redefines species biosynthetic potential |
| topic | Pangenome analysis Streptomyces Genome mining Biosynthetic Gene Clusters Phylogenetic analysis Metabolism |
| url | https://doi.org/10.1186/s13059-024-03471-9 |
| work_keys_str_mv | AT omkarsmohite pangenomeminingofthestreptomycesgenusredefinesspeciesbiosyntheticpotential AT tuesjørgensen pangenomeminingofthestreptomycesgenusredefinesspeciesbiosyntheticpotential AT thomasjbooth pangenomeminingofthestreptomycesgenusredefinesspeciesbiosyntheticpotential AT pepcharusanti pangenomeminingofthestreptomycesgenusredefinesspeciesbiosyntheticpotential AT patrickvphaneuf pangenomeminingofthestreptomycesgenusredefinesspeciesbiosyntheticpotential AT tilmannweber pangenomeminingofthestreptomycesgenusredefinesspeciesbiosyntheticpotential AT bernhardopalsson pangenomeminingofthestreptomycesgenusredefinesspeciesbiosyntheticpotential |