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Within-Species Genomic Variation and Variable Patterns of Recombination in the Tetracycline Producer Streptomyces rimosus.

ABSTRACT: Streptomyces rimosus is best known as the primary source of the tetracycline class of antibiotics, most notably oxytetracycline, which have been widely used against many gram-positive and gram-negative pathogens and protozoan parasites. However, despite the medical and agricultural importance of S. rimosus, little is known of its evolutionary history and genome dynamics. In this study, we aim to elucidate the pan-genome characteristics and phylogenetic relationships of 32 S. rimosus genomes. The S. rimosus pan-genome contains more than 22,000 orthologous gene clusters, and approximately 8.8% of these genes constitutes the core genome. A large part of the accessory genome is composed of 9,646 strain-specific genes. S. rimosus exhibits an open pan-genome (decay parameter α = 0.83) and high gene diversity between strains (genomic fluidity φ = 0.12). We also observed strain-level variation in the distribution and abundance of biosynthetic gene clusters (BGCs) and that each individual S. rimosus genome has a unique repertoire of BGCs. Lastly, we observed variation in recombination, with some strains donating or receiving DNA more often than others, strains that tend to frequently recombine with specific partners, genes that often experience recombination more than others, and variable sizes of recombined DNA sequences. We conclude that the high levels of inter-strain genomic variation in S. rimosus is partly explained by differences in recombination among strains. These results have important implications on current efforts for natural drug discovery, the ecological role of strain-level variation in microbial populations, and addressing the fundamental question of why microbes have pan-genomes.

SUBMITTER: Park CJ

PROVIDER: S-EPMC6437091 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Streptomyces rimosus is an industrial streptomycete, best known as a producer of oxytetracycline, one of the most widely used antibiotics. Despite the significant contribution of Streptomyces species to the pharmaceutical industry, most omics analyses have only been conducted on the model organism Streptomyces coelicolor. In recent years, protein phosphorylation on serine, threonine, and tyrosine (Ser, Thr, and Tyr, respectively) has been shown to play a crucial role in the regulation of numerous cellular processes, including metabolic changes leading to antibiotic production and morphological changes. In this study, we performed a comprehensive quantitative (phospho)proteomic analysis during the growth of S. rimosus under conditions of oxytetracycline production and pellet fragmentation. Liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis combined with phosphopeptide enrichment detected a total of 3,725 proteins, corresponding to 45.6% of the proteome and 417 phosphorylation sites from 230 phosphoproteins. Significant changes in abundance during three distinct growth phases were determined for 494 proteins and 98 phosphorylation sites. Functional analysis revealed changes in phosphorylation events of proteins involved in important cellular processes, including regulatory mechanisms, primary and secondary metabolism, cell division, and stress response. About 80% of the phosphoproteins detected during submerged growth of S. rimosus have not yet been reported in streptomycetes, and 55 phosphoproteins were not reported in any prokaryote studied so far. This enabled the creation of a unique resource that provides novel insights into the dynamics of (phospho)proteins and reveals many potential regulatory events during antibiotic production in liquid culture of an industrially important bacterium. IMPORTANCE Streptomyces rimosus is best known as a primary source of oxytetracycline (OTC). The significant global market value of OTC highlights the need for a better understanding of the regulatory mechanisms that lead to production of this antibiotic. Our study provides, for the first time, a detailed insight into the dynamics of (phospho)proteomic profiles during growth and antibiotic production in liquid culture of S. rimosus. Significant changes in protein synthesis and phosphorylation have been revealed for a number of important cellular proteins during the growth stages that coincide with OTC production and morphological changes of this industrially important bacterium. Most of these proteins have not been detected in previous studies. Therefore, our results significantly expand the insight into phosphorylation events associated with important cellular processes and antibiotic production; they also greatly increase the phosphoproteome of streptomycetes and contribute with newly discovered phosphoproteins to the database of prokaryotic phosphoproteomes. This can consequently lead to the design of novel research directions in elucidation of the complex regulatory network in Streptomyces.

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Within-Species Genomic Variation and Variable Patterns of Recombination in the Tetracycline Producer Streptomyces rimosus.

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