Envelope Control of Outer Membrane Vesicle Production in Gram-Negative Bacteria

Schwechheimer, Carmen; Sullivan, Claretta J.; Kuehn, Meta J.

doi:10.1021/bi400164t

Cited by 143 publications

(176 citation statements)

References 94 publications

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“…6C). We examined two other hypervesiculation mutants (10,15) to ensure that this observed ratio decrease is not simply a general hypervesiculation phenomenon but is instead specific to ⌬degP, and this indeed turned out to be the case (see Fig. S6A in the supplemental material).…”

Section: Figmentioning

confidence: 98%

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Synthetic Effect between Envelope Stress and Lack of Outer Membrane Vesicle Production in Escherichia coli

Schwechheimer

Kuehn

2013

Journal of Bacteriology

109

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Outer membrane vesicles (OMVs) are composed of outer membrane and periplasmic components and are ubiquitously secreted by Gram-negative bacteria. OMVs can disseminate virulence factors for pathogenic bacteria as well as serve as an envelope stress response. From a transposon mutant screen for OMV phenotypes, it was discovered that an nlpA mutant of Escherichia coli produces fewer OMVs than the wild type, whereas a degP mutant produces higher levels of OMVs. NlpA is an inner-membrane-anchored lipoprotein that has a minor role in methionine import. DegP is a periplasmic chaperone/protease for misfolded envelope proteins that is critical when cells are heat shocked. To reveal how these proteins contribute to OMV production, the mutations were combined and the double mutant analyzed. The ⌬nlpA ⌬degP strain displayed a high-temperature growth defect that corresponded to the production of fewer OMVs than produced by the ⌬degP strain. This phenotype also pertained to other undervesiculation mutations in a ⌬degP background. The hypovesiculation phenotype of ⌬nlpA in the wild-type strain as well as in the degP deletion strain was found to be a stationary-phase phenomenon. The periplasm of the ⌬nlpA ⌬degP strain was determined to contain significantly more protein in stationary phase than the wild type. Additionally, misfolded DegP substrate outer membrane porins were detected in ⌬degP mutant-derived OMVs. These data suggest that an accumulation of envelope proteins resulting from decreased vesiculation was toxic and contributed to the growth defect. We conclude that OMV production contributes to relieve the envelope of accumulated toxic proteins and that NlpA plays an important role in the production of vesicles in stationary phase.

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Section: Figmentioning

confidence: 98%

“…They are defined as outer membrane (OM) buds entrapping periplasmic content in the lumen (9). As visualized by electron and atomic force microscopy, OMVs are spherical structures with a diameter ranging from 50 to 250 nm (6,10). OMVs are a means by which Gram-negative bacteria interact with their environment.…”

mentioning

confidence: 99%

Synthetic Effect between Envelope Stress and Lack of Outer Membrane Vesicle Production in Escherichia coli

Schwechheimer

Kuehn

2013

Journal of Bacteriology

109

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“…In E. coli and other bacteria, members of the E regulon, such as chaperones and proteases, ensure the efficient transport of properly folded proteins to the outer membrane. During extracytoplasmic stress, the levels of vesicle formation in E. coli and Pseudomonas aeruginosa change in response to the increased or decreased activity of either E or specific members of its regulon, such as the protease DegP (54)(55)(56). During oxygen limitation and the time of nanowire production, S. oneidensis rpoE has roughly 2-fold increased expression (Fig.…”

Section: Fig 6 Representation Of the Alignment Of Known E Coli Crp-bmentioning

confidence: 99%

Regulation of Gene Expression in Shewanella oneidensis MR-1 during Electron Acceptor Limitation and Bacterial Nanowire Formation

Barchinger

Pirbadian

Sambles

et al. 2016

Appl Environ Microbiol

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In limiting oxygen as an electron acceptor, the dissimilatory metal-reducing bacterium Shewanella oneidensis MR-1 rapidly forms nanowires, extensions of its outer membrane containing the cytochromes MtrC and OmcA needed for extracellular electron transfer. RNA sequencing (RNA-Seq) analysis was employed to determine differential gene expression over time from triplicate chemostat cultures that were limited for oxygen. We identified 465 genes with decreased expression and 677 genes with increased expression. The coordinated increased expression of heme biosynthesis, cytochrome maturation, and transport pathways indicates that S. oneidensis MR-1 increases cytochrome production, including the transcription of genes encoding MtrA, MtrC, and OmcA, and transports these decaheme cytochromes across the cytoplasmic membrane during electron acceptor limitation and nanowire formation. In contrast, the expression of the mtrA and mtrC homologs mtrF and mtrD either remains unaffected or decreases under these conditions. The ompW gene, encoding a small outer membrane porin, has 40-fold higher expression during oxygen limitation, and it is proposed that OmpW plays a role in cation transport to maintain electrical neutrality during electron transfer. The genes encoding the anaerobic respiration regulator cyclic AMP receptor protein (CRP) and the extracytoplasmic function sigma factor RpoE are among the transcription factor genes with increased expression. RpoE might function by signaling the initial response to oxygen limitation. Our results show that RpoE activates transcription from promoters upstream of mtrC and omcA. The transcriptome and mutant analyses of S. oneidensis MR-1 nanowire production are consistent with independent regulatory mechanisms for extending the outer membrane into tubular structures and for ensuring the electron transfer function of the nanowires. IMPORTANCEShewanella oneidensis MR-1 has the capacity to transfer electrons to its external surface using extensions of the outer membrane called bacterial nanowires. These bacterial nanowires link the cell's respiratory chain to external surfaces, including oxidized metals important in bioremediation, and explain why S. oneidensis can be utilized as a component of microbial fuel cells, a form of renewable energy. In this work, we use differential gene expression analysis to focus on which genes function to produce the nanowires and promote extracellular electron transfer during oxygen limitation. Among the genes that are expressed at high levels are those encoding cytochrome proteins necessary for electron transfer. Shewanella coordinates the increased expression of regulators, metabolic pathways, and transport pathways to ensure that cytochromes efficiently transfer electrons along the nanowires.

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“…The precise mechanisms of EV biogenesis and cargo loading are beginning to be identified. Gram-negative bacteria produce EVs (also called outer membrane vesicles) when the outer membrane is "pinched," and the vesicle buds from the cell surface (62). A second vesicle release mechanism is reported to occur within biofilms of P. aeruginosa (63).…”

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confidence: 99%

Multifaceted Interfaces of Bacterial Competition

2016

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bMicrobial communities span many orders of magnitude, ranging in scale from hundreds of cells on a single particle of soil to billions of cells within the lumen of the gastrointestinal tract. Bacterial cells in all habitats are members of densely populated local environments that facilitate competition between neighboring cells. Accordingly, bacteria require dynamic systems to respond to the competitive challenges and the fluctuations in environmental circumstances that tax their fitness. The assemblage of bacteria into communities provides an environment where competitive mechanisms are developed into new strategies for survival. In this minireview, we highlight a number of mechanisms used by bacteria to compete between species. We focus on recent discoveries that illustrate the dynamic and multifaceted functions used in bacterial competition and discuss how specific mechanisms provide a foundation for understanding bacterial community development and function.

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Envelope Control of Outer Membrane Vesicle Production in Gram-Negative Bacteria

Cited by 143 publications

References 94 publications

Synthetic Effect between Envelope Stress and Lack of Outer Membrane Vesicle Production in Escherichia coli

Synthetic Effect between Envelope Stress and Lack of Outer Membrane Vesicle Production in Escherichia coli

Regulation of Gene Expression in Shewanella oneidensis MR-1 during Electron Acceptor Limitation and Bacterial Nanowire Formation

Multifaceted Interfaces of Bacterial Competition

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