Phage Genes Induce Quorum Sensing Signal Release through Membrane Vesicle Formation

Yasuda, Marina; Yamamoto, Tatsuya; Nagakubo, Toshiki; Morinaga, Kana; Obana, Nozomu; Nomura, Nobuhiko; Toyofuku, Masanori

doi:10.1264/jsme2.me21067

Cited by 8 publications

(6 citation statements)

References 48 publications

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“…The effects of the different processes of explosive cell lysis on the composition of MVs has yet to be clarified. Explosive cell lysis in P. denitrificans was previously shown to stimulate the release of C16-HSL due to an increase in the formation of MVs (Yasuda et al, 2022). This finding indicates that a prophage gene interferes with bacterial communication through MV formation, providing insights into the interplay between phages and bacteria.…”

Section: Explosive Cell Lysis Stimulates Signal Release Through MV Fo...mentioning

confidence: 81%

“…MV formation in P. denitrificans is poorly understood; however, a recent study showed that at least genes encoded in the prophage region induced MV formation through explosive cell lysis, in which MVs were also found to be highly enriched in phage DNA (Yasuda et al, 2022). Explosive cell lysis was initially demonstrated in P. aeruginosa, in which peptidoglycan was degraded by endolysin, resulting in cells shattering their membrane, which then rounded up to form MVs (Turnbull et al, 2016).…”

Section: Explosive Cell Lysis Stimulates Signal Release Through MV Fo...mentioning

confidence: 99%

“…As cells lyse, their cytoplasmic contents are released, including DNA, which function as the extracellular matrix in biofilm formation (Turnbull et al, 2016). P. aeruginosa changes from rod-shaped to round cells prior to lysis (Turnbull et al, 2016), whereas P. denitrificans mainly lyses as rods (Yasuda et al, 2022), suggesting that both are triggered by peptidoglycan degradation; however, this process differs among species (Fig. 1).…”

Section: Explosive Cell Lysis Stimulates Signal Release Through MV Fo...mentioning

confidence: 99%

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A Single Shot of Vesicles

2022

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Bacteria communicate through signaling molecules that coordinate group behavior. Hydrophobic signals that do not diffuse in aqueous environments are used as signaling molecules by several bacteria. However, limited information is currently available on the mechanisms by which these molecules are transported between cells. Membrane vesicles (MVs) with diverse functions play important roles in the release and delivery of hydrophobic signaling molecules, leading to differences in the dynamics of signal transportation from those of free diffusion. Studies on Paracoccus denitrificans, which produces a hydrophobic long-chain N-acyl homoserine lactone (AHL), showed that signals were loaded into MVs at a concentration with the potential to trigger the quorum sensing (QS) response with a "single shot" to the cell. Furthermore, stimulating the formation of MVs increased the release of signals from the cell; therefore, a basic understanding of MV formation is important. Novel findings revealed the formation of MVs through different routes, resulting in the production of different types of MVs. Methods such as high-speed atomic force microscopy (AFM) phase imaging allow the physical properties of MVs to be analyzed at a nanometer resolution, revealing their heterogeneity. In this special minireview, we introduce the role of MVs in bacterial communication and highlight recent findings on MV formation and their physical heterogeneity by referring to our research. We hope that this minireview will provide basic information for understanding the functionality of MVs in ecological systems.

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Section: Explosive Cell Lysis Stimulates Signal Release Through MV Fo...mentioning

confidence: 81%

Section: Explosive Cell Lysis Stimulates Signal Release Through MV Fo...mentioning

confidence: 99%

Section: Explosive Cell Lysis Stimulates Signal Release Through MV Fo...mentioning

confidence: 99%

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A Single Shot of Vesicles

2022

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“…Phage-induced lysis of bacterial cells is supposed to contribute extensively to the formation of membrane vesicles in nature [42]. This raises the possibility that membrane vesicles may serve as a defense mechanism by transporting signaling molecules such as quorum sensing molecules in a concentrated manner, as has been observed in Paracoccus denitrificans [43,44]. This could help bacteria communicate and coordinate their defense against phages more effectively.…”

Section: Membrane Vesiclesmentioning

confidence: 95%

Bacterial multicellular behavior in antiviral defense

Luthe¹,

Kever²,

Thormann³

et al. 2023

Preprint

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Multicellular behaviour benefits seemingly simple organisms such as bacteria, by improving nutrient uptake, resistance to stresses or by providing advantages in predatory interactions. Several recent studies have shown that this also extends to the defense against bacteriophages, which are omnipresent in almost all habitats. In this review, we summarize strategies conferring protection against phage infection at the multicellular level, covering secretion of small antiphage molecules or membrane vesicles, the role of quorum sensing in phage defense, and the impact of biofilm components and architecture. Recent studies focusing on these topics push the boundaries of our understanding of the bacterial immune system and set the ground for an appreciation of bacterial multicellular behaviour in antiviral defense.

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“…Past reports have demonstrated interactions between these two biocolloids. For instance, EVs prevent phage infection of bacteria , or serve as collectors for phage, whereas phage can induce the increased production of EVs. , Due to similarities in physical–chemical properties, however, EVs and phages can be difficult to distinguish. An example of this difficulty is highlighted in studies of seawater.…”

Section: Extracellular Vesicles As Functional Colloids In the Environ...mentioning

confidence: 99%

Extracellular Vesicles and Bacteriophages: New Directions in Environmental Biocolloid Research

Hicks,

Rogers,

Hendren

et al. 2023

Environ. Sci. Technol.

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There is a long-standing appreciation among environmental engineers and scientists regarding the importance of biologically derived colloidal particles and their environmental fate. This interest has been recently renewed in considering bacteriophages and extracellular vesicles, which are each poised to offer engineers unique insights into fundamental aspects of environmental microbiology and novel approaches for engineering applications, including advances in wastewater treatment and sustainable agricultural practices. Challenges persist due to our limited understanding of interactions between these nanoscale particles with unique surface properties and their local environments. This review considers these biological particles through the lens of colloid science with attention given to their environmental impact and surface properties. We discuss methods developed for the study of inert (nonbiological) particle–particle interactions and the potential to use these to advance our understanding of the environmental fate and transport of extracellular vesicles and bacteriophages.

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Phage Genes Induce Quorum Sensing Signal Release through Membrane Vesicle Formation

Cited by 8 publications

References 48 publications

A Single Shot of Vesicles

A Single Shot of Vesicles

Bacterial multicellular behavior in antiviral defense

Extracellular Vesicles and Bacteriophages: New Directions in Environmental Biocolloid Research

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