Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles

Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles

2010 | Adam Kulp and Meta J. Kuehn
Outer membrane vesicles (OMVs) are secreted by Gram-negative bacteria and contain biologically active proteins and lipids. Unlike other secretion mechanisms, OMVs enable bacteria to secrete both soluble and insoluble molecules. OMVs allow enzymes to reach distant targets in a concentrated, protected, and targeted form. They also play roles in bacterial survival, such as nutrient acquisition, biofilm development, and pathogenesis. Key characteristics of OMV biogenesis include outward bulging of areas lacking membrane-peptidoglycan bonds, the ability to upregulate vesicle production without losing outer membrane integrity, enrichment or exclusion of certain proteins and lipids, and membrane fission without direct energy from ATP/GTP hydrolysis. Comparisons of similar budding mechanisms from diverse biological domains have provided new insights into OMV biogenesis. OMVs are small spherical structures 20–250 nm in diameter produced when portions of the outer membrane bulge away from the cell, pinch off, and release. Soluble proteins are associated with OMVs as entrapped periplasmic material and externally adherent material. OMVs can disseminate far from the cell and impart biological functions on the environment and on other cells, including playing a role in pathogenesis, quorum signaling, nutrient acquisition, and horizontal gene transfer. OMV production is a common feature of all Gram-negative bacteria, and because of the energy cost implicit in replacing the shed lipids and proteins, OMV formation has presumably evolved for a reason. Studies of OMVs have focused on their composition, functions, conditions affecting production, and the design of OMV-based vaccines. Although several mechanisms for vesiculation have been proposed, there is little concerted evidence supporting these ideas. It is possible that vesiculation occurs by a well-conserved mechanism; however, different types of OMVs may exist and originate by different mechanisms. Understanding how bacteria produce OMVs can help us comprehend how other domains of life produce similar secreted structures, and vice versa. Such comparisons will yield insight into the general principles involved in forming a vesicle from a biological membrane. OMVs are a secretion and delivery system in that they can disseminate bacterial products and interact with the environment. OMV-mediated secretion can be regulated temporally and spatially. However, OMV secretion is distinct from the better-studied soluble protein secretion systems. In OMV secretion, soluble material is released in a complex with and/or surrounded by insoluble material. By contrast, soluble secretory pathways export specific monomeric or small protein complexes, and secretion is not accompanied by the release of other cellular material. OMVs can reach a distant site in a hostile environment with an active, specific, and/or highly concentrated cohort of molecules, and they can also be specifically targeted to a particular distal site through the binding specificity between surface-exposed bacterial adhesins and environmental ligands or receptors. The combination of these characteristics makes OMV secretion particularly effectiveOuter membrane vesicles (OMVs) are secreted by Gram-negative bacteria and contain biologically active proteins and lipids. Unlike other secretion mechanisms, OMVs enable bacteria to secrete both soluble and insoluble molecules. OMVs allow enzymes to reach distant targets in a concentrated, protected, and targeted form. They also play roles in bacterial survival, such as nutrient acquisition, biofilm development, and pathogenesis. Key characteristics of OMV biogenesis include outward bulging of areas lacking membrane-peptidoglycan bonds, the ability to upregulate vesicle production without losing outer membrane integrity, enrichment or exclusion of certain proteins and lipids, and membrane fission without direct energy from ATP/GTP hydrolysis. Comparisons of similar budding mechanisms from diverse biological domains have provided new insights into OMV biogenesis. OMVs are small spherical structures 20–250 nm in diameter produced when portions of the outer membrane bulge away from the cell, pinch off, and release. Soluble proteins are associated with OMVs as entrapped periplasmic material and externally adherent material. OMVs can disseminate far from the cell and impart biological functions on the environment and on other cells, including playing a role in pathogenesis, quorum signaling, nutrient acquisition, and horizontal gene transfer. OMV production is a common feature of all Gram-negative bacteria, and because of the energy cost implicit in replacing the shed lipids and proteins, OMV formation has presumably evolved for a reason. Studies of OMVs have focused on their composition, functions, conditions affecting production, and the design of OMV-based vaccines. Although several mechanisms for vesiculation have been proposed, there is little concerted evidence supporting these ideas. It is possible that vesiculation occurs by a well-conserved mechanism; however, different types of OMVs may exist and originate by different mechanisms. Understanding how bacteria produce OMVs can help us comprehend how other domains of life produce similar secreted structures, and vice versa. Such comparisons will yield insight into the general principles involved in forming a vesicle from a biological membrane. OMVs are a secretion and delivery system in that they can disseminate bacterial products and interact with the environment. OMV-mediated secretion can be regulated temporally and spatially. However, OMV secretion is distinct from the better-studied soluble protein secretion systems. In OMV secretion, soluble material is released in a complex with and/or surrounded by insoluble material. By contrast, soluble secretory pathways export specific monomeric or small protein complexes, and secretion is not accompanied by the release of other cellular material. OMVs can reach a distant site in a hostile environment with an active, specific, and/or highly concentrated cohort of molecules, and they can also be specifically targeted to a particular distal site through the binding specificity between surface-exposed bacterial adhesins and environmental ligands or receptors. The combination of these characteristics makes OMV secretion particularly effective
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