Bacterial Outer Membrane Vesicles: From Discovery to Applications

2021 ◽  
Vol 75 (1) ◽  
Author(s):  
Mariana G. Sartorio ◽  
Evan J. Pardue ◽  
Mario F. Feldman ◽  
M. Florencia Haurat
Keyword(s):  
Outer Membrane ◽  
Stress Responses ◽  
Current Knowledge ◽  
Cell Communication ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Multiple Roles ◽  
Annual Review ◽  
Publication Date ◽  
Cellular Components

Secretion of cellular components across the plasma membrane is an essential process that enables organisms to interact with their environments. Production of extracellular vesicles in bacteria is a well-documented but poorly understood process. Outer membrane vesicles (OMVs) are produced in gram-negative bacteria by blebbing of the outer membrane. In addition to their roles in pathogenesis, cell-to-cell communication, and stress responses, OMVs play important roles in immunomodulation and the establishment and balance of the gut microbiota. In this review, we discuss the multiple roles of OMVs and the current knowledge of OMV biogenesis. We also discuss the growing and promising biotechnological applications of OMV. Expected final online publication date for the Annual Review of Microbiology, Volume 75 is October 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

scholarly journals Bacterial Outer Membrane Vesicles Induce Plant Immune Responses

2016 ◽  
Vol 29 (5) ◽  
pp. 374-384 ◽  
Author(s):  
Ofir Bahar ◽  
Gideon Mordukhovich ◽  
Dee Dee Luu ◽  
Benjamin Schwessinger ◽  
Arsalan Daudi ◽  
...  
Keyword(s):  
Immune Response ◽  
Outer Membrane ◽  
Plant Pathogens ◽  
Cell Communication ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Defense Gene Expression ◽  
Defense Gene ◽  
Bacterial Communication ◽  
Multiple Processes

Gram-negative bacteria continuously pinch off portions of their outer membrane, releasing membrane vesicles. These outer membrane vesicles (OMVs) are involved in multiple processes including cell-to-cell communication, biofilm formation, stress tolerance, horizontal gene transfer, and virulence. OMVs are also known modulators of the mammalian immune response. Despite the well-documented role of OMVs in mammalian-bacterial communication, their interaction with plants is not well studied. To examine whether OMVs of plant pathogens modulate the plant immune response, we purified OMVs from four different plant pathogens and used them to treat Arabidopsis thaliana. OMVs rapidly induced a reactive oxygen species burst, medium alkalinization, and defense gene expression in A. thaliana leaf discs, cell cultures, and seedlings, respectively. Western blot analysis revealed that EF-Tu is present in OMVs and that it serves as an elicitor of the plant immune response in this form. Our results further show that the immune coreceptors BAK1 and SOBIR1 mediate OMV perception and response. Taken together, our results demonstrate that plants can detect and respond to OMV-associated molecules by activation of their immune system, revealing a new facet of plant-bacterial interactions.

scholarly journals Sex Steroids Induce Membrane Stress Responses and Virulence Properties in Pseudomonas aeruginosa

mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Celine Vidaillac ◽  
Valerie Fei Lee Yong ◽  
Marie-Stephanie Aschtgen ◽  
Jing Qu ◽  
Shuowei Yang ◽  
...  
Keyword(s):  
Cystic Fibrosis ◽  
Pseudomonas Aeruginosa ◽  
Outer Membrane ◽  
Stress Responses ◽  
Sex Steroids ◽  
Respiratory Diseases ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Membrane Stress ◽  
Content Type

ABSTRACT Estrogen, a major female sex steroid hormone, has been shown to promote the selection of mucoid Pseudomonas aeruginosa in the airways of patients with chronic respiratory diseases, including cystic fibrosis. This results in long-term persistence, poorer clinical outcomes, and limited therapeutic options. In this study, we demonstrate that at physiological concentrations, sex steroids, including testosterone and estriol, induce membrane stress responses in P. aeruginosa. This is characterized by increased virulence and consequent inflammation and release of proinflammatory outer membrane vesicles promoting in vivo persistence of the bacteria. The steroid-induced P. aeruginosa response correlates with the molecular polarity of the hormones and membrane fluidic properties of the bacteria. This novel mechanism of interaction between sex steroids and P. aeruginosa explicates the reported increased disease severity observed in females with cystic fibrosis and provides evidence for the therapeutic potential of the modulation of sex steroids to achieve better clinical outcomes in patients with hormone-responsive strains. IMPORTANCE Molecular mechanisms by which sex steroids interact with P. aeruginosa to modulate its virulence have yet to be reported. Our work provides the first characterization of a steroid-induced membrane stress mechanism promoting P. aeruginosa virulence, which includes the release of proinflammatory outer membrane vesicles, resulting in inflammation, host tissue damage, and reduced bacterial clearance. We further demonstrate that at nanomolar (physiological) concentrations, male and female sex steroids promote virulence in clinical strains of P. aeruginosa based on their dynamic membrane fluidic properties. This work provides, for the first-time, mechanistic insight to better understand and predict the P. aeruginosa related response to sex steroids and explain the interindividual patient variability observed in respiratory diseases such as cystic fibrosis that are complicated by gender differences and chronic P. aeruginosa infection.

scholarly journals Outer Membrane Vesicle Induction and Isolation for Vaccine Development

2021 ◽  
Vol 12 ◽  
Author(s):  
Melanie D. Balhuizen ◽  
Edwin J. A. Veldhuizen ◽  
Henk P. Haagsman
Keyword(s):  
Outer Membrane ◽  
Vaccine Development ◽  
Current Knowledge ◽  
Membrane Vesicle ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Gram Negative Bacteria ◽  
Bacterial Surface ◽  
Advantages And Disadvantages ◽  
Isolation Methods

Gram-negative bacteria release vesicular structures from their outer membrane, so called outer membrane vesicles (OMVs). OMVs have a variety of functions such as waste disposal, communication, and antigen or toxin delivery. These vesicles are the promising structures for vaccine development since OMVs carry many surface antigens that are identical to the bacterial surface. However, isolation is often difficult and results in low yields. Several methods to enhance OMV yield exist, but these do affect the resulting OMVs. In this review, our current knowledge about OMVs will be presented. Different methods to induce OMVs will be reviewed and their advantages and disadvantages will be discussed. The effects of the induction and isolation methods used in several immunological studies on OMVs will be compared. Finally, the challenges for OMV-based vaccine development will be examined and one example of a successful OMV-based vaccine will be presented.

scholarly journals Elicitation of Epithelial Cell-Derived Immune Effectors by Outer Membrane Vesicles of Nontypeable Haemophilus influenzae

2011 ◽  
Vol 79 (11) ◽  
pp. 4361-4369 ◽  
Author(s):  
Samantha W. Sharpe ◽  
Meta J. Kuehn ◽  
Kevin M. Mason
Keyword(s):  
Epithelial Cells ◽  
Haemophilus Influenzae ◽  
Antimicrobial Peptide ◽  
Outer Membrane ◽  
Stress Responses ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Virulence Determinants ◽  
Nontypeable Haemophilus Influenzae ◽  
Content Type

ABSTRACTOuter membrane vesicles (OMVs) are produced by all Gram-negative microorganisms studied to date. The contributions of OMVs to biological processes are diverse and include mediation of bacterial stress responses, selective packaging and secretion of virulence determinants, modulation of the host immune response, and contributions to biofilm formation and stability. First characterized as transformasomes inHaemophilus, these membranous blebs facilitate transfer of DNA among bacteria. NontypeableHaemophilus influenzae(NTHI), an opportunistic pathogen of the upper and lower respiratory tracts, produces OMVsin vivo, but there is a paucity of information regarding both the composition and role of OMVs during NTHI colonization and pathogenesis. We demonstrated that purified NTHI vesicles are 20 to 200 nm in diameter and contain DNA, adhesin P5, IgA endopeptidase, serine protease, and heme utilization protein, suggesting a multifaceted role in virulence. NTHI OMVs can bind to human pharyngeal epithelial cells, resulting in a time- and temperature-dependent aggregation on the host cell surface, with subsequent internalization. OMVs colocalize with the endocytosis protein caveolin, indicating that internalization is mediated by caveolae, which are cholesterol-rich lipid raft domains. Upon interaction with epithelial cells, NTHI OMVs stimulate significant release of the immunomodulatory cytokine interleukin-8 (IL-8) as well as the antimicrobial peptide LL-37. Thus, we demonstrated that NTHI OMVs contain virulence-associated proteins that dynamically interact with and invade host epithelial cells. Beyond their ability to mediate DNA transfer inHaemophilus, OMV stimulation of host immunomodulatory cytokine and antimicrobial peptide release supports a dynamic role for vesiculation in NTHI pathogenesis and clinically relevant disease progression.

scholarly journals Outer Membrane Vesicles of Gram-Negative Bacteria: An Outlook on Biogenesis

2021 ◽  
Vol 12 ◽  
Author(s):  
Eric Daniel Avila-Calderón ◽  
María del Socorro Ruiz-Palma ◽  
Ma. Guadalupe Aguilera-Arreola ◽  
Norma Velázquez-Guadarrama ◽  
Enrico A. Ruiz ◽  
...  
Keyword(s):  
Membrane Proteins ◽  
Quorum Sensing ◽  
Outer Membrane ◽  
Molecular Mechanisms ◽  
Outer Membrane Proteins ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Gram Negative Bacteria ◽  
Gram Negative ◽  
Cellular Components

Outer membrane vesicles (OMVs) from Gram-negative bacteria were first described more than 50 years ago. However, the molecular mechanisms involved in biogenesis began to be studied only in the last few decades. Presently, the biogenesis and molecular mechanisms for their release are not completely known. This review covers the most recent information on cellular components involved in OMV biogenesis, such as lipoproteins and outer membrane proteins, lipopolysaccharide, phospholipids, quorum-sensing molecules, and flagella.

scholarly journals Helicobacter pylori-Derived Outer Membrane Vesicles (OMVs): Role in Bacterial Pathogenesis?

2020 ◽  
Vol 8 (9) ◽  
pp. 1328 ◽  
Author(s):  
Miroslaw Jarzab ◽  
Gernot Posselt ◽  
Nicole Meisner-Kober ◽  
Silja Wessler
Keyword(s):  
Helicobacter Pylori ◽  
Outer Membrane ◽  
Current Knowledge ◽  
Membrane Vesicles ◽  
Bacterial Pathogenesis ◽  
Outer Membrane Vesicles ◽  
Host Cells ◽  
Cellular Mechanisms ◽  
Wide Range ◽  
H Pylori

Persistent infections with the human pathogen Helicobacter pylori (H. pylori) have been closely associated with the induction and progression of a wide range of gastric disorders, including acute and chronic gastritis, ulceration in the stomach and duodenum, mucosa-associated lymphoid tissue (MALT) lymphoma, and gastric adenocarcinoma. The pathogenesis of H. pylori is determined by a complicated network of manifold mechanisms of pathogen–host interactions, which involves a coordinated interplay of H. pylori pathogenicity and virulence factors with host cells. While these molecular and cellular mechanisms have been intensively investigated to date, the knowledge about outer membrane vesicles (OMVs) derived from H. pylori and their implication in bacterial pathogenesis is not well developed. In this review, we summarize the current knowledge on H. pylori-derived OMVs.

Prokaryotic membrane vesicles: new insights on biogenesis and biological roles

2015 ◽  
Vol 396 (2) ◽  
pp. 95-109 ◽  
Author(s):  
M. Florencia Haurat ◽  
Wael Elhenawy ◽  
Mario F. Feldman
Keyword(s):  
Stress Response ◽  
Gut Microbiota ◽  
Outer Membrane ◽  
Recent Work ◽  
Cell Communication ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Gram Negative Bacteria ◽  
Gram Negative ◽  
Gram Positive Bacteria

Abstract Biogenesis and trafficking of membrane vesicles are essential and well-studied processes in eukaryotes. In contrast, vesiculation in bacteria is not well understood. Outer membrane vesicles (OMVs) are produced in Gram-negative bacteria by blebbing of the outer membrane. In addition to the roles in pathogenesis, cell-to-cell communication and stress response, recent work has suggested that OMVs play important roles in immunomodulation and the establishment and balance of the gut microbiota. In this review we discuss the known and novel roles of OMVs and the different biogenesis models proposed, and address the evidence for cargo selection into OMVs. We also discuss the growing evidence for the existence of membrane vesicles in Gram-positive bacteria and Archaea. Due to their biological importance and promising applications in vaccinology, the biogenesis of OMVs is an important topic in microbiology.

scholarly journals Abiotic stressors impact outer membrane vesicle composition in a beneficial rhizobacterium: Raman spectroscopy characterization

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Matthew Potter ◽  
Cynthia Hanson ◽  
Anne J. Anderson ◽  
Elizabeth Vargis ◽  
David W. Britt
Keyword(s):  
Raman Spectroscopy ◽  
Nucleic Acids ◽  
Outer Membrane ◽  
Stress Responses ◽  
Membrane Vesicle ◽  
Plant Stress ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Linear Discriminant ◽  
Abiotic Stressors

AbstractOuter membrane vesicles (OMVs) produced by Gram-negative bacteria have roles in cell-to-cell signaling, biofilm formation, and stress responses. Here, the effects of abiotic stressors on OMV contents and composition from biofilm cells of the plant health-promoting bacterium Pseudomonas chlororaphis O6 (PcO6) are examined. Two stressors relevant to this root-colonizing bacterium were examined: CuO nanoparticles (NPs)-a potential fertilizer and fungicide- and H2O2-released from roots during plant stress responses. Atomic force microscopy revealed 40–300 nm diameter OMVs from control and stressed biofilm cells. Raman spectroscopy with linear discriminant analysis (LDA) was used to identify changes in chemical profiles of PcO6 cells and resultant OMVs according to the cellular stressor with 84.7% and 83.3% accuracies, respectively. All OMVs had higher relative concentrations of proteins, lipids, and nucleic acids than PcO6 cells. The nucleic acid concentration in OMVs exhibited a cellular stressor-dependent increase: CuO NP-induced OMVs > H2O2-induced OMVs > control OMVs. Biochemical assays confirmed the presence of lipopolysaccharides, nucleic acids, and protein in OMVs; however, these assays did not discriminate OMV composition according to the cellular stressor. These results demonstrate the sensitivity of Raman spectroscopy using LDA to characterize and distinguish cellular stress effects on OMVs composition and contents.

scholarly journals A Suppressor of Cell Death Caused by the Loss of σE Downregulates Extracytoplasmic Stress Responses and Outer Membrane Vesicle Production in Escherichia coli

2006 ◽  
Vol 189 (5) ◽  
pp. 1523-1530 ◽  
Author(s):  
Julie E. Button ◽  
Thomas J. Silhavy ◽  
Natividad Ruiz
Keyword(s):  
Escherichia Coli ◽  
Cell Death ◽  
Outer Membrane ◽  
Stress Responses ◽  
Membrane Vesicle ◽  
Membrane Vesicles ◽  
Outer Membrane Vesicles ◽  
Loss Of Function ◽  
Gene Encoding ◽  
Σ Factor

ABSTRACT When envelope biogenesis is compromised or damage to envelope components occurs, bacteria trigger signaling cascades, which lead to the production of proteins that combat such extracytoplasmic stresses. In Escherichia coli, there are three pathways known to deal with envelope stresses: the Bae, Cpx, and σE responses. Although the effectors of the Bae and Cpx responses are not essential in E. coli, the effector of the σE response, the sigma factor RpoE (σE), is essential for viability. However, mutations that suppress the lethality of an rpoE-null allele can be easily obtained, and here we describe how we have isolated at least four classes of these suppressors. We present the first description of one such suppressor class, loss-of-function mutations in ydcQ, a gene encoding a putative DNA-binding protein. In wild-type rpoE + strains, ydcQ mutants have two distinct phenotypes: extracytoplasmic stress responses are significantly downregulated, and the production of outer membrane vesicles is severely reduced. We present a model in which σE is not essential per se but, rather, we propose that rpoE mutant cells die, possibly because they overreact to the absence of this σ factor by triggering a cell death signal.

Sign in / Sign up

Export Citation Format

Share Document