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Angucyclines as signals modulate the behaviors of Streptomyces coelicolor.

ABSTRACT: The angucycline antibiotic jadomycin B (JdB) produced by Streptomyces venezuelae has been found here to induce complex survival responses in Streptomyces coelicolor at subinhibitory concentration. The receptor for JdB was identified as a "pseudo" gamma-butyrolactone receptor, ScbR2, which was shown to bind two previously unidentified target promoters, those of redD (redDp) and adpA (adpAp), thus directly regulating undecylprodigiosin (Red) production and morphological differentiation, respectively. Because AdpA also directly regulates the expression of redD, ScbR2, AdpA, and RedD together form a feed-forward loop controlling both differentiation and Red production phenotypes. Different signal strengths (i.e., JdB concentrations) were shown to induce the two different phenotypes by modulating the relative transcription levels of adpA vs. redD. The induction of morphological differentiation and endogenous antibiotic production by exogenous antibiotic exemplifies an important survival strategy more sophisticated than the induction of antibiotic resistance.

SUBMITTER: Wang W

PROVIDER: S-EPMC3992645 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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Angucyclines as signals modulate the behaviors of Streptomyces coelicolor.

Wang Weishan W Ji Junjie J Li Xiao X Wang Juan J Li Shanshan S Pan Guohui G Fan Keqiang K Yang Keqian K

Proceedings of the National Academy of Sciences of the United States of America 20140328 15

The angucycline antibiotic jadomycin B (JdB) produced by Streptomyces venezuelae has been found here to induce complex survival responses in Streptomyces coelicolor at subinhibitory concentration. The receptor for JdB was identified as a "pseudo" gamma-butyrolactone receptor, ScbR2, which was shown to bind two previously unidentified target promoters, those of redD (redDp) and adpA (adpAp), thus directly regulating undecylprodigiosin (Red) production and morphological differentiation, respective ...[more]

PMID: 24706927

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Project description:Nucleoid-associated proteins (NAPs) are small, highly abundant transcriptional regulators with low sequence specificity which are involved in multiple DNA-related processes including gene expression, DNA protection, recombination/repair and nucleoid structuring. Through these functions they are able to regulate important phenotypic properties including virulence, secondary metabolism and stress resistance. However the set of NAPs known within the Actinobacteria is small and incomplete. The missing proteins are likely to be key regulators of virulence in pathogens such as Mycobacterium tuberculosis and also of development and secondary metabolism in industrially-important species such as Streptomyces. Here, we use label-free LC-MS/MS to systematically search for novel NAPs in isolated nucleoids of the model actinomycete Streptomyces coelicolor. Based on the criteria of high abundance (emPAI score) and predicted DNA-binding ability (DNAbinder score) we identified a set of 24 proteins with a high predicted likelihood of being NAPs. The approach was deemed successful as the set included known major NAPs HupA, HupS, sIHF and Lsr2 as well as the global transcriptional regulators BldD and CRP and the pleiotropic response regulator AfsQ1. It also included a number of proteins whose functions are not yet known from recognisable classes of transcription factor (SCO2140, SCO4493, SCO1839, SCO1210, SCO5405, SCO4229, SCO3198) or from uncharacterised protein families (SCO5783, SCO5592, SCO3793, SCO6482) which comprise a valuable set of candidates for further study.In this paper we establish a robust protocol for preparing S. coelicolor nucleoids for mass spectrometric analysis and develop a workflow for identifying novel nucleoid-associated proteins (NAPs) by combining LC-MS/MS with a bioinformatical analysis. The nucleoid-associated proteins of many species are known to be key regulators of virulence, stress tolerance and global patterns of gene expression. Identifying the "missing" nucleoid proteins of S. coelicolor is likely to have important implications for manipulating the production of secondary metabolites such as antibiotics. Candidate NAPs were identified. Several of these are highly conserved in clinically important species such as Mycobacterium and in many commercially important species such as Salinispora and Micromonospora which represent a vital source of novel drugs such as antibiotics, antifungals and anticancer agents.

Dataset Information

Angucyclines as signals modulate the behaviors of Streptomyces coelicolor.

Publications

Angucyclines as signals modulate the behaviors of Streptomyces coelicolor.

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