Most cited article - PubMed ID 892668
Macromolecular synthesis accompanying the transition from spores to vegetative forms of Streptomyces granaticolor
Spore awakening is a series of actions that starts with purely physical processes and continues via the launching of gene expression and metabolic activities, eventually achieving a vegetative phase of growth. In spore-forming microorganisms, the germination process is controlled by intra- and inter-species communication. However, in the Streptomyces clade, which is capable of developing a plethora of valuable compounds, the chemical signals produced during germination have not been systematically studied before. Our previously published data revealed that several secondary metabolite biosynthetic genes are expressed during germination. Therefore, we focus here on the secondary metabolite production during this developmental stage. Using high-performance liquid chromatography-mass spectrometry, we found that the sesquiterpenoid antibiotic albaflavenone, the polyketide germicidin A, and chalcone are produced during germination of the model streptomycete, S. coelicolor. Interestingly, the last two compounds revealed an inhibitory effect on the germination process. The secondary metabolites originating from the early stage of microbial growth may coordinate the development of the producer (quorum sensing) and/or play a role in competitive microflora repression (quorum quenching) in their nature environments.
- Keywords
- Streptomyces, albaflavenone, cell signaling, chalcone, germicidin, secondary metabolism, spore germination,
- Publication type
- Journal Article MeSH
The complex development undergone by Streptomyces encompasses transitions from vegetative mycelial forms to reproductive aerial hyphae that differentiate into chains of single-celled spores. Whereas their mycelial life - connected with spore formation and antibiotic production - is deeply investigated, spore germination as the counterpoint in their life cycle has received much less attention. Still, germination represents a system of transformation from metabolic zero point to a new living lap. There are several aspects of germination that may attract our attention: (1) Dormant spores are strikingly well-prepared for the future metabolic restart; they possess stable transcriptome, hydrolytic enzymes, chaperones, and other required macromolecules stabilized in a trehalose milieu; (2) Germination itself is a specific sequence of events leading to a complete morphological remodeling that include spore swelling, cell wall reconstruction, and eventually germ tube emergences; (3) Still not fully unveiled are the strategies that enable the process, including a single cell's signal transduction and gene expression control, as well as intercellular communication and the probability of germination across the whole population. This review summarizes our current knowledge about the germination process in Streptomyces, while focusing on the aforementioned points.
- Keywords
- Streptomyces, cell wall, dormancy, gene expression, germination, metabolism, signaling, spore,
- Publication type
- Journal Article MeSH
- Review MeSH
BACKGROUND: Bacterial spore germination is a developmental process during which all required metabolic pathways are restored to transfer cells from their dormant state into vegetative growth. Streptomyces are soil dwelling filamentous bacteria with complex life cycle, studied mostly for they ability to synthesize secondary metabolites including antibiotics. RESULTS: Here, we present a systematic approach that analyzes gene expression data obtained from 13 time points taken over 5.5 h of Streptomyces germination. Genes whose expression was significantly enhanced/diminished during the time-course were identified, and classified to metabolic and regulatory pathways. The classification into metabolic pathways revealed timing of the activation of specific pathways during the course of germination. The analysis also identified remarkable changes in the expression of specific sigma factors over the course of germination. Based on our knowledge of the targets of these factors, we speculate on their possible roles during germination. Among the factors whose expression was enhanced during the initial part of germination, SigE is though to manage cell wall reconstruction, SigR controls protein re-aggregation, and others (SigH, SigB, SigI, SigJ) control osmotic and oxidative stress responses. CONCLUSIONS: From the results, we conclude that most of the metabolic pathway mRNAs required for the initial phases of germination were synthesized during the sporulation process and stably conserved in the spore. After rehydration in growth medium, the stored mRNAs are being degraded and resynthesized during first hour. From the analysis of sigma factors we conclude that conditions favoring germination evoke stress-like cell responses.
- MeSH
- Bacterial Proteins genetics metabolism MeSH
- Time Factors MeSH
- Heat-Shock Response genetics MeSH
- Gene Expression Profiling * MeSH
- Streptomyces coelicolor genetics growth & development metabolism physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Bacterial Proteins MeSH
Streptomycetes have been studied mostly as producers of secondary metabolites, while the transition from dormant spores to an exponentially growing culture has largely been ignored. Here, we focus on a comparative analysis of fluorescently and radioactively labeled proteome and microarray acquired transcriptome expressed during the germination of Streptomyces coelicolor. The time-dynamics is considered, starting from dormant spores through 5.5 hours of growth with 13 time points. Time series of the gene expressions were analyzed using correlation, principal components analysis and an analysis of coding genes utilization. Principal component analysis was used to identify principal kinetic trends in gene expression and the corresponding genes driving S. coelicolor germination. In contrast with the correlation analysis, global trends in the gene/protein expression reflected by the first principal components showed that the prominent patterns in both the protein and the mRNA domains are surprisingly well correlated. Analysis of the number of expressed genes identified functional groups activated during different time intervals of the germination.
- MeSH
- Principal Component Analysis MeSH
- Energy Metabolism genetics MeSH
- Phenotype MeSH
- Stress, Physiological genetics MeSH
- Gene Regulatory Networks MeSH
- Metabolic Networks and Pathways MeSH
- Proteome * MeSH
- Gene Expression Regulation, Bacterial * MeSH
- Spores, Bacterial genetics metabolism MeSH
- Streptomyces coelicolor genetics metabolism ultrastructure MeSH
- Transcriptome * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Proteome * MeSH
- MeSH
- Anti-Bacterial Agents biosynthesis MeSH
- Bacteria growth & development metabolism MeSH
- Bacterial Proteins metabolism MeSH
- RNA, Bacterial metabolism MeSH
- DNA, Bacterial metabolism MeSH
- DNA metabolism MeSH
- Fungi growth & development metabolism MeSH
- RNA metabolism MeSH
- Spores, Bacterial physiology MeSH
- Streptomyces growth & development metabolism MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Anti-Bacterial Agents MeSH
- Bacterial Proteins MeSH
- RNA, Bacterial MeSH
- DNA, Bacterial MeSH
- DNA MeSH
- RNA MeSH
Nonfilamentous forms of Streptomyces granaticolor are formed in a medium with amino acids and glucose. They form filaments again after transfer to a medium with glucose and peptone. The nonfilamentous forms do not produce granaticin. Formation of nonfilamentous forms depends on the concentration of the inoculum, on the cultivation temperature and on the presence of simple sugars. Ultrathin sections revealed atypical septation in the nonmycelial forms and non-uniform accumulation of the wall material.
- MeSH
- Culture Media MeSH
- Streptomyces growth & development ultrastructure MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Culture Media MeSH