The σ
            <sup>E</sup>
            Cell Envelope Stress Response of
            <i>Streptomyces coelicolor</i>
            Is Influenced by a Novel Lipoprotein, CseA

Hutchings, Matthew I.; Hong, Hee‐Jeon; Leibovitz, Emmanuelle; Sutcliffe, Iain C.; Buttner, Mark J.

doi:10.1128/jb.00818-06

Cited by 51 publications

(41 citation statements)

References 42 publications

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“…E is part of a signal transduction system sensing certain changes in the integrity of the cell envelope (24) and transcribing the cwg operon putatively involved in cell wall glycan synthesis (23). The phenotype of a E mutant, with an altered cell wall structure and increased sensitivity to cell wall-lytic enzymes, resembled somewhat that of the ⌬mreB mutant (37,39).…”

Section: Discussionmentioning

confidence: 99%

The MreB-Like Protein Mbl ofStreptomyces coelicolorA3(2) Depends on MreB for Proper Localization and Contributes to Spore Wall Synthesis

et al. 2011

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Most bacteria with a rod-shaped morphology contain an actin-like cytoskeleton consisting of MreB polymers, which form helical spirals underneath the cytoplasmic membrane to direct peptidoglycan synthesis for the elongation of the cell wall. In contrast, MreB of Streptomyces coelicolor is not required for vegetative growth but has a role in sporulation. Besides MreB, S. coelicolor encodes two further MreB-like proteins, Mbl and SCO6166, whose function is unknown. Whereas MreB and Mbl are highly similar, SCO6166 is shorter, lacking the subdomains IB and IIB of actin-like proteins. Here, we showed that MreB and Mbl are not functionally redundant but cooperate in spore wall synthesis. Expression analysis by semiquantitative reverse transcription-PCR revealed distinct expression patterns. mreB and mbl are induced predominantly during morphological differentiation. In contrast, sco6166 is strongly expressed during vegetative growth but switched off during sporulation. All genes could be deleted without affecting viability. Even a ⌬mreB ⌬mbl double mutant was viable. ⌬sco6166 had a wild-type phenotype. ⌬mreB, ⌬mbl, and ⌬mreB ⌬mbl produced swollen, prematurely germinating spores that were sensitive to various kinds of stress, suggesting a defect in spore wall integrity. During aerial mycelium formation, an Mbl-mCherry fusion protein colocalized with an MreB-enhanced green fluorescent protein (MreB-eGFP) fusion protein at the sporulation septa. Whereas MreB-eGFP localized properly in the ⌬mbl mutant, Mbl-mCherry localization depended on the presence of a functional MreB protein. Our results revealed that MreB and Mbl cooperate in the synthesis of the thickened spore wall, while SCO6166 has a nonessential function during vegetative growth.The peptidoglycan (PG) layer, consisting of long glycan strands cross-linked by short peptides, is a major determinant of bacterial cell shape (51). Most species with a complex, nonspherical morphology contain the actin-like MreB protein, which belongs to the HSP70-actin-sugar kinase (ASHKA) superfamily of proteins (4, 48). MreB was shown to polymerize into a dynamic helical filament underneath the cytoplasmic membrane spanning the long axis of the cells (11,17,25,30,33). In rod-shaped bacteria, MreB is thought to interact with other proteins to position a cell wall-synthesizing complex at the lateral cell wall (16,17,32). The incorporation of new PG at the lateral wall results in cell elongation, thus determining rod-shaped morphology. Gram-negative bacteria seem to have a single mreB gene, usually in an operon with mreC and mreD.

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Section: Discussionmentioning

confidence: 99%

The MreB-Like Protein Mbl ofStreptomyces coelicolorA3(2) Depends on MreB for Proper Localization and Contributes to Spore Wall Synthesis

et al. 2011

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“…In addition to the sensing of peptides described earlier, lipoproteins have roles in cell envelope sensing processes, including the modulation of two-component signal transduction systems [44,69,70] and the Bacillus germinant receptors GerAC, GerBC, GerD and GerKC [46,71]. Moreover, genome analyses have consistently identified putative lipoproteins predicted to have important roles in cell envelope stability and cell wall cross-linking or remodelling such as penicillin binding proteins and peptidoglycan hydrolases [18,54].…”

Section: Bioinformatic Prediction Of Lipoproteins In Grampositive Bacmentioning

confidence: 99%

Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold ‘em, knowing when to fold ‘em

Hutchings

Palmer

Harrington

et al. 2009

Trends in Microbiology

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181

219

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“…Thus, PspQ could function in concert with PspEF as a self-resistance mechanism against planosporicin. Interestingly, the lipoprotein CseA negatively regulates the ECF sigma factor E in Streptomyces coelicolor (55). The proximity of pspQ to pspXW in P. alba, and similar gene arrangements in other known or putative lantibiotic biosynthetic gene clusters (in N. brasiliensis, M. corallina, and Thermobispora bispora), may indicate a role for PspQ in regulating PspX.…”

Section: Identification Of P Alba As a Planosporicin Producer Fourmentioning

confidence: 99%

Cloning and Analysis of the Planosporicin Lantibiotic Biosynthetic Gene Cluster of Planomonospora alba

2013

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The increasing prevalence of antibiotic resistance in bacterial pathogens has renewed focus on natural products with antimicrobial properties. Lantibiotics are ribosomally synthesized peptide antibiotics that are posttranslationally modified to introduce (methyl)lanthionine bridges. Actinomycetes are renowned for their ability to produce a large variety of antibiotics, many with clinical applications, but are known to make only a few lantibiotics. One such compound is planosporicin produced by Planomonospora alba, which inhibits cell wall biosynthesis in Gram-positive pathogens. Planosporicin is a type AI lantibiotic structurally similar to those which bind lipid II, the immediate precursor for cell wall biosynthesis. The gene cluster responsible for planosporicin biosynthesis was identified by genome mining and subsequently isolated from a P. alba cosmid library. A minimal cluster of 15 genes sufficient for planosporicin production was defined by heterologous expression in Nonomuraea sp. strain ATCC 39727, while deletion of the gene encoding the precursor peptide from P. alba, which abolished planosporicin production, was also used to confirm the identity of the gene cluster. Deletion of genes encoding likely biosynthetic enzymes identified through bioinformatic analysis revealed that they, too, are essential for planosporicin production in the native host. Reverse transcription-PCR (RT-PCR) analysis indicated that the planosporicin gene cluster is transcribed in three operons. Expression of one of these, pspEF, which encodes an ABC transporter, in Streptomyces coelicolor A3(2) conferred some degree of planosporicin resistance on the heterologous host. The inability to delete these genes from P. alba suggests that they play an essential role in immunity in the natural producer.

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The σ ^E Cell Envelope Stress Response of Streptomyces coelicolor Is Influenced by a Novel Lipoprotein, CseA

Cited by 51 publications

References 42 publications

The MreB-Like Protein Mbl ofStreptomyces coelicolorA3(2) Depends on MreB for Proper Localization and Contributes to Spore Wall Synthesis

The MreB-Like Protein Mbl ofStreptomyces coelicolorA3(2) Depends on MreB for Proper Localization and Contributes to Spore Wall Synthesis

Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold ‘em, knowing when to fold ‘em

Cloning and Analysis of the Planosporicin Lantibiotic Biosynthetic Gene Cluster of Planomonospora alba

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The σ E Cell Envelope Stress Response of Streptomyces coelicolor Is Influenced by a Novel Lipoprotein, CseA

Cited by 51 publications

References 42 publications

The MreB-Like Protein Mbl ofStreptomyces coelicolorA3(2) Depends on MreB for Proper Localization and Contributes to Spore Wall Synthesis

The MreB-Like Protein Mbl ofStreptomyces coelicolorA3(2) Depends on MreB for Proper Localization and Contributes to Spore Wall Synthesis

Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold ‘em, knowing when to fold ‘em

Cloning and Analysis of the Planosporicin Lantibiotic Biosynthetic Gene Cluster of Planomonospora alba

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The σ ^E Cell Envelope Stress Response of Streptomyces coelicolor Is Influenced by a Novel Lipoprotein, CseA