Changes in glycogen and trehalose content of<i>Streptomyces brasiliensis</i>hyphae during growth in liquid cultures under sporulating and non-sporulating conditions

Rueda, Begoña; Miguélez, Elisa M.; Hardisson, Carlos; Manzanal, Manuel B.

doi:10.1111/j.1574-6968.2001.tb09466.x

Cited by 34 publications

(17 citation statements)

References 12 publications

(14 reference statements)

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“…Ribosomes and storage granules were observed throughout vegetative hyphae ( Figure 3A). The storage granules in S. albus were likely composed of glycogen as glycogen has been shown to accumulate during vegetative growth to fuel sporulation in other streptomycetes (Brana et al, 1986;Rueda et al, 2001). We observed a 6-nm wide layer ∼10 nm underneath the cytoplasmic membrane at hyphal tips that was not detected elsewhere in the vegetative hyphae ( Figure 3A, inset and Supplementary Movie S2).…”

Section: Features Of Vegetative Hyphaementioning

confidence: 80%

Ultrastructure of Exospore Formation in Streptomyces Revealed by Cryo-Electron Tomography

Sexton

Tocheva

2020

Front. Microbiol.

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Many bacteria form spores in response to adverse environmental conditions. Several sporulation pathways have evolved independently and occur through distinctive mechanisms. Here, using cryo-electron tomography (cryo-ET), we examine all stages of growth and exospore formation in the model organism Streptomyces albus. Our data reveal the native ultrastructure of vegetative hyphae, including the likely structures of the polarisome and cytoskeletal filaments. In addition, we observed septal junctions in vegetative septa, predicted to be involved in protein and DNA translocation between neighboring cells. During sporulation, the cell envelope undergoes dramatic remodeling, including the formation of a spore wall and two protective proteinaceous layers. Mature spores reveal the presence of a continuous spore coat and an irregular rodlet sheet. Together, these results provide an unprecedented examination of the ultrastructure in Streptomyces and further our understanding of the structural complexity of exospore formation.

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Section: Features Of Vegetative Hyphaementioning

confidence: 80%

Ultrastructure of Exospore Formation in Streptomyces Revealed by Cryo-Electron Tomography

Sexton

Tocheva

2020

Front. Microbiol.

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“…4), encodes the metabolic enzyme TreZ, which functions in a pathway that breaks down the storage compound glycogen to yield trehalose (74). The accumulation and degradation of glycogen, stored as insoluble granules, are under developmental control in Streptomyces , and glycogen reserves are actively degraded during sporulation (75, 76), leading to an accumulation of trehalose that contributes substantially to the heat and desiccation resistance of mature spores (77). Thus, the activation of treZ transcription by WhiA (see Table S1 in the supplemental material) provides a direct link between the regulatory cascade that controls differentiation in Streptomyces and the accumulation of trehalose in spores.…”

Section: Resultsmentioning

confidence: 99%

Genes Required for Aerial Growth, Cell Division, and Chromosome Segregation Are Targets of WhiA before Sporulation in Streptomyces venezuelae

Bush

Bibb

Chandra

et al. 2013

mBio

110

156

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WhiA is a highly unusual transcriptional regulator related to a family of eukaryotic homing endonucleases. WhiA is required for sporulation in the filamentous bacterium Streptomyces, but WhiA homologues of unknown function are also found throughout the Gram-positive bacteria. To better understand the role of WhiA in Streptomyces development and its function as a transcription factor, we identified the WhiA regulon through a combination of chromatin immunoprecipitation-sequencing (ChIP-seq) and microarray transcriptional profiling, exploiting a new model organism for the genus, Streptomyces venezuelae, which sporulates in liquid culture. The regulon encompasses ~240 transcription units, and WhiA appears to function almost equally as an activator and as a repressor. Bioinformatic analysis of the upstream regions of the complete regulon, combined with DNase I footprinting, identified a short but highly conserved asymmetric sequence, GACAC, associated with the majority of WhiA targets. Construction of a null mutant showed that whiA is required for the initiation of sporulation septation and chromosome segregation in S. venezuelae, and several genes encoding key proteins of the Streptomyces cell division machinery, such as ftsZ, ftsW, and ftsK, were found to be directly activated by WhiA during development. Several other genes encoding proteins with important roles in development were also identified as WhiA targets, including the sporulation-specific sigma factor σWhiG and the diguanylate cyclase CdgB. Cell division is tightly coordinated with the orderly arrest of apical growth in the sporogenic cell, and filP, encoding a key component of the polarisome that directs apical growth, is a direct target for WhiA-mediated repression during sporulation.

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“…During the analysis of 169 manually reviewed sequences, we also found that the bacterial set includes several multi-copy GBEs. Studies show that multi-copy GBEs contribute to bacterial physiology and glycogen metabolism in a differentially spatial and temporal manner (Bruton et al, 1995; Schneider et al, 2000; Rueda et al, 2001). Thus, it is also worth further experimental study in terms of their classifications, distributions and functions to better understand glycogen metabolism in bacteria.…”

Section: Discussionmentioning

confidence: 99%

Structure and Evolution of Glycogen Branching Enzyme N-Termini From Bacteria

Wang

Liu

et al. 2019

Front. Microbiol.

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In bacteria, glycogen plays important roles in carbon and energy storage. Its structure has recently been linked with bacterial environmental durability. Among the essential genes for bacterial glycogen metabolism, the glgB-encoded branching enzyme GBE plays an essential role in forming α-1,6-glycosidic branching points, and determines the unique branching patterns in glycogen. Previously, evolutionary analysis of a small sets of GBEs based on their N-terminal domain organization revealed that two types of GBEs might exist: (1) Type 1 GBE with both N1 and N2 (also known as CBM48) domains and (2) Type 2 GBE with only the N2 domain. In this study, we initially analyzed N-terminal domains of 169 manually reviewed bacterial GBEs based on hidden Markov models. A previously unreported group of GBEs (Type 3) with around 100 amino acids ahead of the N1 domains was identified. Phylogenetic analysis found clustered patterns of GBE types in certain bacterial phyla, with the shorter, Type 2 GBEs predominantly found in Gram-positive species, while the longer Type 1 GBEs are found in Gram-negative species. Several in vitro studies have linked N1 domain with transfer of short oligosaccharide chains during glycogen formation, which could lead to small and compact glycogen structures. Compact glycogen degrades more slowly and, as a result, may serve as a durable energy reserve, contributing to the enhanced environmental persistence for bacteria. We were therefore interested in classifying GBEs based on their N-terminal domain via large-scale sequence analysis. In addition, we set to understand the evolutionary patterns of different GBEs through phylogenetic analysis at species and sequence levels. Three-dimensional modeling of GBE N-termini was also performed for structural comparisons. A further study of 9,387 GBE sequences identified 147 GBEs that might belong to a possibly novel group of Type 3 GBE, most of which fall into the phylum of Actinobacteria. We also attempted to correlate glycogen average chain length (ACL) with GBE types. However, no significant conclusions were drawn due to limited data availability. In sum, our study systematically investigated bacterial GBEs in terms of domain organizations from evolutionary point of view, which provides guidance for further experimental study of GBE N-terminal functions in glycogen structure and bacterial physiology.

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Changes in glycogen and trehalose content ofStreptomyces brasiliensishyphae during growth in liquid cultures under sporulating and non-sporulating conditions

Cited by 34 publications

References 12 publications

Ultrastructure of Exospore Formation in Streptomyces Revealed by Cryo-Electron Tomography

Ultrastructure of Exospore Formation in Streptomyces Revealed by Cryo-Electron Tomography

Genes Required for Aerial Growth, Cell Division, and Chromosome Segregation Are Targets of WhiA before Sporulation in Streptomyces venezuelae

Structure and Evolution of Glycogen Branching Enzyme N-Termini From Bacteria

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