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Composition and functions of bacterial membrane vesicles

Nature Reviews Microbiology volume 21, pages 415–430 (2023)Cite this article

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Abstract

Extracellular vesicles are produced by species across all domains of life, suggesting that vesiculation represents a fundamental principle of living matter. In Gram-negative bacteria, membrane vesicles (MVs) can originate either from blebs of the outer membrane or from endolysin-triggered explosive cell lysis, which is often induced by genotoxic stress. Although less is known about the mechanisms of vesiculation in Gram-positive and Gram-neutral bacteria, recent research has shown that both lysis and blebbing mechanisms also exist in these organisms. Evidence has accumulated over the past years that different biogenesis routes lead to distinct types of MV with varied structure and composition. In this Review, we discuss the different types of MV and their potential cargo packaging mechanisms. We summarize current knowledge regarding how MV composition determines their various functions including support of bacterial growth via the disposal of waste material, nutrient scavenging, export of bioactive molecules, DNA transfer, neutralization of phages, antibiotics and bactericidal functions, delivery of virulence factors and toxins to host cells and inflammatory and immunomodulatory effects. We also discuss the advantages of MV-mediated secretion compared with classic bacterial secretion systems and we introduce the concept of quantal secretion.

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Fig. 1: Membrane vesicle types with different structures and compositions have different biogenesis routes.
Fig. 2: Membrane vesicle cargo transport and delivery.
Fig. 3: Membrane vesicles as quantal delivery systems.
Fig. 4: Membrane vesicles have diverse biological functions.
Fig. 5: Bacterial membrane vesicles enter host cells to modulate immunity and mediate pathogenesis.

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Acknowledgements

M.T. was supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) (projects 19H05682 and 19H02866), the Suntory Rising Stars Encouragement Program in Life Sciences (SunRiSE) and the Japan Science and Technology Agency ERATO (JPMJER1502), S.S. was supported by the Austrian Science Fund (FWF) (grants P 33073 and P 32577), M.K.-L. was supported by the Australian Research Council (Discovery Project DP190101655) and by a veski Inspiring Women Fellowship, and L.E. was supported by the Swiss National Science Foundation (SNSF) (projects 310030_192800 and CRSII5_186410).

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Authors and Affiliations

  1. Faculty of Life and Environmental Sciences, Microbiology Research Center for Sustainability, University of Tsukuba, Tsukuba, Japan

    Masanori Toyofuku

  2. Institute of Molecular Biosciences–Infection Biology, University of Graz, Graz, Austria

    Stefan Schild

  3. BioTechMed Graz, Graz, Austria

    Stefan Schild

  4. Field of Excellence BioHealth, University of Graz, Graz, Austria

    Stefan Schild

  5. Department of Microbiology, Anatomy, Physiology and Pharmacology, La Trobe University, Melbourne, Victoria, Australia

    Maria Kaparakis-Liaskos

  6. Research Centre for Extracellular Vesicles, La Trobe University, Melbourne, Victoria, Australia

    Maria Kaparakis-Liaskos

  7. Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland

    Leo Eberl

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Glossary

Bistable gene expression

A regulatory system that results in the same gene being expressed in some cells and silenced in others to trigger stochastic switch-like transitions between cellular differentiation states.

Endolysins

Hydrolytic enzymes that are produced by bacteriophages to degrade the cell wall of the bacterial host during the final stage of the lytic cycle.

Intercalation

Reversible insertion of molecules into materials with layered structures such as the cellular membrane.

Pattern recognition receptors

PRRs. Germline-encoded innate immune receptors expressed by macrophages, dendritic cells and epithelial cells that recognize different types of pathogen-associated molecular pattern.

Quantal secretion

Secretion of molecule packages to ensure biological activity on delivery to target cells.

Quorum sensing

QS. A cell-to-cell communication mechanism in bacteria by which gene regulation is controlled in a population-dependent manner through the production and perception of signal molecules.

SOS response

A global regulatory system that allows bacteria to respond to DNA damage by arresting growth and inducing DNA repair and mutagenesis as well as controlling prophage induction.

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Toyofuku, M., Schild, S., Kaparakis-Liaskos, M. et al. Composition and functions of bacterial membrane vesicles. Nat Rev Microbiol 21, 415–430 (2023). https://doi.org/10.1038/s41579-023-00875-5

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