Abstract
BackgroundStreptomycetes are filamentous soil-dwelling bacteria. They are best known as the producers of a great variety of natural products such as antibiotics, antifungals, antiparasitics, and anticancer agents and the decomposers of organic substances for carbon recycling. They are also model organisms for the studies of gene regulatory networks, morphological differentiation, and stress response. The availability of sets of genomes from closely related Streptomyces strains makes it possible to assess the mechanisms underlying genome plasticity and systems adaptation.ResultsWe present the results of a comprehensive analysis of the genomes of five Streptomyces species with distinct phenotypes. These streptomycetes have a pan-genome comprised of 17,362 orthologous families which includes 3,096 components in the core genome, 5,066 components in the dispensable genome, and 9,200 components that are uniquely present in only one species. The core genome makes up about 33%-45% of each genome repertoire. It contains important genes for Streptomyces biology including those involved in gene regulation, secretion, secondary metabolism and morphological differentiation. Abundant duplicate genes have been identified, with 4%-11% of the whole genomes composed of lineage-specific expansions (LSEs), suggesting that frequent gene duplication or lateral gene transfer events play a role in shaping the genome diversification within this genus. Two patterns of expansion, single gene expansion and chromosome block expansion are observed, representing different scales of duplication.ConclusionsOur results provide a catalog of genome components and their potential functional roles in gene regulatory networks and metabolic networks. The core genome components reveal the minimum requirement for streptomycetes to sustain a successful lifecycle in the soil environment, reflecting the effects of both genome evolution and environmental stress acting upon the expressed phenotypes. A better understanding of the LSE gene families will, on the other hand, bring a wealth of new insights into the mechanisms underlying strain-specific phenotypes, such as the production of novel antibiotics, pathogenesis, and adaptive response to environmental challenges.
Highlights
We report a comprehensive comparative genomic analysis of five model species in the genus Streptomyces [3,6,19,20,21] with complete genome sequences and annotation [22]: (1) S. coelicolor is a model organism for streptomycetes and it can produce a variety of antibiotics, including actinorhodin, CDA, methylenomycin, and undecylprodigiosin [23]; (2) S. avermitilis [6] produces avermectin which is a potent agent against a wide array of nematodes and arthropod parasites; (3) S. griseus [20] produces streptomycin, a broad-spectrum antibiotic which has been used for the treatment of various diseases such as tuberculosis and the plague caused by Yersinia pestis [24,25]
AfsK/ AfsR system plays multiple roles in Streptomyces biology; it was shown to be a key regulator of secondary metabolism in S. coelicolor, and essential for morphological differentiation in S. griseus [51]. While they remain to be defined [50], the roles of master regulators-sigma factors in secondary metabolism have begun to be unraveled by several independent research groups: Zhuo et al [52] showed that mutation of a house-keeping sigma factor HrdB enhanced the production of avermectins in S. avermitilis; we previously reported that SigK [53] and SigT [54] were both involved in the regulation of antibiotic production and morphological development in S. coelicolor
Comparative genomic analysis of the five Streptomyces species revealed a pan-genome with 17,362 orthologous families which includes 3,096 components in the core genome, 5,066 components in the dispensable genome, and 9,200 components that are uniquely present in only one species
Summary
They are best known as the producers of a great variety of natural products such as antibiotics, antifungals, antiparasitics, and anticancer agents and the decomposers of organic substances for carbon recycling. They are model organisms for the studies of gene regulatory networks, morphological differentiation, and stress response. Streptomyces is a group of Gram positive bacteria ubiquitously inhabiting soil It is the largest genus in the Actinobacteria, including over 580 species [1]. The genome sequence of the second species in this genus, S. avermitilis, an industrial strain for avermectin production, was released in 2003 [6]. At the time of writing, the genome sequencing projects of about 30 Streptomyces strains are in various stages of completion
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