Taxonomic and biosynthetic diversity of the marine actinomycete Salinispora across spatial scales

海洋放线菌 Salinispora 在不同空间尺度上的分类和生物合成多样性

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Abstract

The spatial scales of bacterial taxonomic and natural product biosynthetic diversity remain poorly understood. This is especially true at the population level, where contrasts between small and large-scale biogeographical patterns are seldom reported. To address these unknowns for the marine actinomycete genus Salinispora, we sequenced the genomes of 99 strains cultured from sediments collected within a 1 m(2) plot (microscale strains). Ninety-six of the microscale strains were identified as S. arenicola, suggesting that this is the most abundant species in the sediments sampled. These strains were assigned to 2 of the 11 populations identified based on 99% ANI among 61 public genomes obtained from 10 global collection sites (global strains). The populations showed evidence of geographic isolation, suggesting that barriers to dispersal or ecological contingencies limit distributions across large spatial scales. An assessment of S. arenicola biosynthetic gene diversity among 157 (combined microscale and global) genomes revealed 100 gene cluster families (GCFs), of which one-third were detected in either one or all strains. Sixty-seven percent of the global GCFs were detected among the microscale strains, indicating that deep sampling from a single location recovered a large percentage of the global biosynthetic diversity. Paired genomic and metabolomic analyses of the microscale strains linked compounds to an orphan PKS-NRPS GCF, while the metabolites ikarugamycin and fridamycin E were identified for the first time from Salinispora. This study provides insight into the diversity and biosynthetic potential of Salinispora at various spatial scales while expanding the collection of natural products reported from the genus. IMPORTANCE: The marine actinomycete genus Salinispora has become a model organism for natural product discovery and to address actinomycete diversity and distributions in marine systems. While biogeographic patterns have been reported at global scales, contrasts have yet to be made with the species diversity that can be recovered from a single location. Here we sequenced the genomes of 96 S. arenicola strains cultured from marine sediments collected within a 1 m(2) plot and compared the diversity detected to public genomes obtained from global collection sites. The results provide evidence of geographic isolation among S. arenicola populations and biosynthetic genes that are mobilized across population boundaries. Multi-omic analyses linked compounds to their respective biosynthetic genes and revealed compounds not previously reported from the genus. This study adds to our growing understanding of Salinispora diversity and biosynthetic potential.

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