Pre-sporulation stages of<i>Streptomyces</i>differentiation: state-of-the-art and future perspectives

Yagüe, Paula; López-García, María Teresa; Rioseras, Beatriz; Sánchez, Jesús; Manteca, Ángel

doi:10.1111/1574-6968.12128

Cited by 65 publications

(60 citation statements)

References 95 publications

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“…Evidence is accumulating that, like eukaryotes, bacteria undergo a process of programmed cell death (PCD). Bacterial multicellularity implies a lifestyle involving cellular heterogeneity and the occasional sacrifice of selected cells for the benefit of survival of the colony (70–72). PCD is likely a major hallmark of multicellularity (8), and has been described in the biofilm-film forming Streptococcus (14) and Bacillus (10), in Myxobacteria that form fruiting bodies (59), in the filamentous cyanobacteria (3, 40), and in the branching Streptomyces (35, 38, 61).…”

Section: Resultsmentioning

confidence: 99%

High-resolution analysis of the peptidoglycan composition inStreptomyces coelicolor

Wezel

Aart

Spijksma

et al. 2018

Preprint

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22The bacterial cell wall maintains cell shape and protects against bursting by the 23 turgor. A major constituent of the cell wall is peptidoglycan (PG), which is 24 continuously modified to allow cell growth and differentiation through the concerted 25 activity of biosynthetic and hydrolytic enzymes. Streptomycetes are Gram-positive 26 bacteria with a complex multicellular life style alternating between mycelial growth 27 and the formation of reproductive spores. This involves cell-wall remodeling at apical 28 sites of the hyphae during cell elongation and autolytic degradation of the vegetative 29 mycelium during the onset of development and antibiotic production. Here, we show 30 that there are distinct differences in the cross-linking and maturation of the PG 31 between exponentially growing vegetative hyphae and the aerial hyphae that 32 undergo sporulation. LC-MS/MS analysis identified over 80 different muropeptides, 33 revealing that major PG hydrolysis takes place over the course of mycelial growth. 34 Half of the dimers lack one of the disaccharide units in transition-phase cells, most 35 likely due to autolytic activity. De-acetylation of MurNAc to MurN was particularly 36 pronounced in spores, suggesting that MurN plays a role in spore development. 37 Taken together, our work highlights dynamic and growth phase-dependent 38 construction and remodeling of PG in Streptomyces. 39 40 IMPORTANCE 41 Streptomycetes are bacteria with a complex lifestyle, which are model organisms for 42 bacterial multicellularity. From a single spore a large multigenomic, multicellular 43 mycelium is formed, which differentiates to form spores. Programmed cell death is an 44 important event during the onset of morphological differentiation. In this work we 45 3 provide new insights into the changes in the peptidoglycan architecture over time, 46 highlighting changes over the course of development and between growing mycelia 47 56 Peptidoglycan (PG) is a major component of the bacterial cell wall. It forms a physical 57boundary that maintains cell shape, protects cellular integrity against the osmotic 58 pressure and acts as a scaffold for large protein assemblies and exopolymers (66). 59The cell wall is a highly dynamic macromolecule that is continuously constructed and 60 deconstructed to allow for cell growth and to meet environmental demands (27). PG 61 is built up of glycan strands of alternating N-acetylglucosamine (GlcNAc) and N-62 acetylmuramic acid (MurNAc) residues that are connected by short peptides to form 63 a mesh-like polymer. PG biosynthesis starts with the synthesis of PG precursors by 64 the Mur enzymes in the cytoplasm and cell membrane, resulting in lipid II precursor, 65 undecaprenylpyrophosphoryl-MurNAc(GlcNAc)-pentapeptide. Lipid II is transported 66 across the cell membrane by MurJ and/or FtsW/SEDS proteins and the PG is 67 polymerized and incorporated into the existing cell wall by the activities of 68 glycosyltransferases and transpeptidases (9, 30, 57). 69 The Gram-positive model bacterium Bacillus ...

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Section: Resultsmentioning

confidence: 99%

High-resolution analysis of the peptidoglycan composition inStreptomyces coelicolor

Wezel

Aart

Spijksma

et al. 2018

Preprint

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“…Cell differentiation is triggered by nutrient depletion and other signals, and both the production of secondary metabolites and morphological differentiation are initiated. whi mutants defective in different sporulation stages are employed in genetic and biochemical analyses of these developmental stages (Yagüe, López‐Garcia, Rioseras, Sánchez, & Manteca, ). The regulation of secondary metabolism in streptomycetes is diverse and complex.…”

Section: Discussionmentioning

confidence: 99%

“…whi mutants defective in different sporulation stages are employed in genetic and biochemical analyses of these developmental stages (Yagüe, López-Garcia, Rioseras, Sánchez, & Manteca, 2013). The regulation of secondary metabolism in streptomycetes is diverse and complex.…”

Section: Discussionmentioning

confidence: 99%

wblE2transcription factor inStreptomyces griseusS4‐7 plays an important role in plant protection

et al. 2017

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Streptomyces griseus S4‐7 was originally isolated from the strawberry rhizosphere as a microbial agent responsible for Fusarium wilt suppressive soils. S. griseus S4‐7 shows specific and pronounced antifungal activity against Fusarium oxysporum f. sp. fragariae. In the Streptomyces genus, the whi transcription factors are regulators of sporulation, cell differentiation, septation, and secondary metabolites production. wblE2 function as a regulator has emerged as a new group in whi transcription factors. In this study, we reveal the involvement of the wblE2 transcription factor in the plant‐protection by S. griseus S4‐7. We generated ΔwblE, ΔwblE2, ΔwhiH, and ΔwhmD gene knock‐out mutants, which showed less antifungal activity both in vitro and in planta. Among the mutants, wblE2 mutant failed to protect the strawberry against the Fusarium wilt pathogen. Transcriptome analyses revealed major differences in the regulation of phenylalanine metabolism, polyketide and siderophore biosynthesis between the S4‐7 and the wblE2 mutant. The results contribute to our understanding of the role of streptomycetes wblE2 genes in a natural disease suppressing system.

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“…A refined investigation showed that the development of vegetative mycelium can be further distinguished into different steps; a young, compartmentalised mycelium undergoes programmed cell death. Viable parts differentiate subsequently into multinucleated second mycelia divided by thin, infrequent and single-layer septa [158][159][160]. Some of these mycelia grow into the air to form aerial mycelia covered by a hydrophobic shell [161,162].…”

Section: Development Of Bacterial Morphologymentioning

confidence: 99%

The Taming of the Shrew - Controlling the Morphology of Filamentous Eukaryotic and Prokaryotic Microorganisms

Walisko

Moench-Tegeder

Blotenberg

et al. 2015

Advances in Biochemical Engineering/Biotechnology

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One of the most sensitive process characteristics in the cultivation of filamentous biological systems is their complex morphology. In submerged cultures, the observed macroscopic morphology of filamentous microorganisms varies from freely dispersed mycelium to dense spherical pellets consisting of a more or less dense, branched and partially intertwined network of hyphae. Recently, the freely dispersed mycelium form has been in high demand for submerged cultivation because this morphology enhances the growth and production of several valuable products. A distinct filamentous morphology and productivity are influenced by the environment and can be controlled by inoculum concentration, spore viability, pH value, cultivation temperature, dissolved oxygen concentration, medium composition, mechanical stress or process mode as well as through the addition of inorganic salts or microparticles, which provides the opportunity to tailor a filamentous morphology. The suitable morphology for a given bioprocess varies depending on the desired product. Therefore, the advantages and disadvantages of each morphological type should be carefully evaluated for every biological system. Because of the high industrial relevance of filamentous microorganisms, research in previous years has aimed at the development of tools and techniques to characterise their growth and obtain quantitative estimates of their morphological properties. The focus of this review is on current advances in the characterisation and control of filamentous morphology with a separation of eukaryotic and prokaryotic systems. Furthermore, recent strategies to tailor the morphology through classical biochemical process parameters, morphology and genetic engineering to optimise the productivity of these filamentous systems are discussed.

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Pre-sporulation stages ofStreptomycesdifferentiation: state-of-the-art and future perspectives

Cited by 65 publications

References 95 publications

High-resolution analysis of the peptidoglycan composition inStreptomyces coelicolor

High-resolution analysis of the peptidoglycan composition inStreptomyces coelicolor

wblE2transcription factor inStreptomyces griseusS4‐7 plays an important role in plant protection

The Taming of the Shrew - Controlling the Morphology of Filamentous Eukaryotic and Prokaryotic Microorganisms

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