Outer Membrane Vesiculation Facilitates Surface Exchange and In Vivo Adaptation of Vibrio cholerae

Zingl, Franz G.; Kohl, Paul; Çakar, Fatih; Leitner, Deborah R.; Mitterer, Fabian; Bonnington, Katherine E.; Rechberger, Gerald; Kuehn, Meta J.; Guan, Ziqiang; Reidl, Joachim; Schild, Stefan

doi:10.1016/j.chom.2019.12.002

Cited by 76 publications

(87 citation statements)

References 70 publications

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“…This is supported by the previous study showing that Haemophilus influenzae released OMVs rich in phosphatidylethanolamine (PE), another typical cone-shaped lipid in bacterial membranes, under iron limitation condition ( Roier et al., 2016 ). Together with our results, this and the related study in Vibrio cholerae ( Zingl et al., 2019 ) suggest that the remodeling membrane lipid compositions and the accumulation of lipids with certain conformational properties may be a key to understanding a common molecular mechanism underlying MV formation across diverse classes of bacteria.…”

Section: Discussionsupporting

confidence: 85%

Mycolic acid-containing bacteria trigger distinct types of membrane vesicles through different routes

et al. 2021

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Section: Discussionsupporting

confidence: 85%

Mycolic acid-containing bacteria trigger distinct types of membrane vesicles through different routes

et al. 2021

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“…Iron limitation, cysteine deficiency, and magnesium depletion are instances of nutrient depletion that promote the general stress response pathways. Inside the hosts, nutrient depletion can also induce pathogen colonization, as well as the expression of virulence factors, followed by the triggering of membrane vesiculation ( Bishop and Work, 1965 ; van de Waterbeemd et al, 2013 ; Zingl et al, 2020 ).…”

Section: Environmental Stressmentioning

confidence: 99%

“…Thus, in the absence of iron, hypervesiculation occurs because membrane asymmetry is disrupted ( Malinverni and Silhavy, 2009 ; Hassan and Troxell, 2013 ). Moreover, at the initial stages of infection when pathogens are faced with iron deficiency in their hosts, they switch off this system so as to better adapt to their host environment via hypervesiculation as well as LPS modification ( Zingl et al, 2020 ).…”

Section: Environmental Stressmentioning

confidence: 99%

“…The presence of nutrient-absorbing molecules on the surface of OMVs induced by starvation enhances the dispersal of these molecules in the environment. Upon nutrient deficiency, the cell downregulates components of the MLA system ( Manning and Kuehn, 2011 ; Zingl et al, 2020 ), resulting in the release of membrane vesicles with nutrient-absorbing molecules such as iron chelators on their surface ( Roier et al, 2016 ; Davies et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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Membrane Vesicle Production as a Bacterial Defense Against Stress

Mozaheb

Mingeot‐Leclercq

2020

Front. Microbiol.

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Membrane vesicles are the nano-sized vesicles originating from membranes. The production of membrane vesicles is a common feature among bacteria. Depending on the bacterial growth phase and environmental conditions, membrane vesicles show diverse characteristics. Various physiological and ecological roles have been attributed to membrane vesicles under both homeostatic and stressful conditions. Pathogens encounter several stressors during colonization in the hostile environment of host tissues. Nutrient deficiency, the presence of antibiotics as well as elements of the host’s immune system are examples of stressors threatening pathogens inside their host. To combat stressors and survive, pathogens have established various defensive mechanisms, one of them is production of membrane vesicles. Pathogens produce membrane vesicles to alleviate the destructive effects of antibiotics or other types of antibacterial treatments. Additionally, membrane vesicles can also provide benefits for the wider bacterial community during infections, through the transfer of resistance or virulence factors. Hence, given that membrane vesicle production may affect the activities of antibacterial agents, their production should be considered when administering antibacterial treatments. Besides, regarding that membrane vesicles play vital roles in bacteria, disrupting their production may suggest an alternative strategy for battling against pathogens. Here, we aim to review the stressors encountered by pathogens and shed light on the roles of membrane vesicles in increasing pathogen adaptabilities in the presence of stress-inducing factors.

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“…In contrast, lack of MlaA promotes virulence in a murine model of Neisseria gonorrhoeae infection ( Baarda et al, 2019 ). Disrupting the Mla system prompts formation of OM vesicles (OMV) for H. influenzae, Vibrio cholerae, N. gonorrhoeae, and A. baumannii ( Baarda et al, 2019 ; Powers and Trent, 2019 ; Roier et al, 2016 ; Zingl et al, 2020 ). The mla genes are transcriptionally regulated by metals ( Baarda et al, 2019 ; Roier et al, 2016 ), and A. baumannii mlaF expression is induced by metal chelation ( Hood et al, 2012 ; Mortensen et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

Modulating Isoprenoid Biosynthesis Increases Lipooligosaccharides and Restores Acinetobacter baumannii Resistance to Host and Antibiotic Stress

et al. 2020

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SUMMARY Acinetobacter baumannii is a leading cause of ventilator-associated pneumonia and a critical threat due to multidrug resistance. The A. baumannii outer membrane is an asymmetric lipid bilayer composed of inner leaflet glycerophospholipids and outer leaflet lipooligosaccharides. Deleting mlaF of the maintenance of lipid asymmetry (Mla) system causes A. baumannii to become more susceptible to pulmonary surfactants and antibiotics and decreases bacterial survival in the lungs of mice. Spontaneous suppressor mutants isolated from infected mice contain an IS Aba11 insertion upstream of the ispB initiation codon, an essential isoprenoid biosynthesis gene. The insertion restores antimicrobial resistance and virulence to Δ mlaF . The suppressor strain increases lipooligosaccharides, suggesting that the mechanism involves balancing the glycerophospholipids/lipooligosaccharides ratio on the bacterial surface. An identical insertion exists in an extensively drug-resistant A. baumannii isolate, demonstrating its clinical relevance. These data show that the stresses bacteria encounter during infection select for genomic rearrangements that increase resistance to antimicrobials.

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Outer Membrane Vesiculation Facilitates Surface Exchange and In Vivo Adaptation of Vibrio cholerae

Abstract: Highlights d Phospholipid transport of Vibrio cholerae is silenced upon host entry d Reduced transporter activity triggers OMV release and increases colonization fitness d Increased vesiculation accelerates modulation of cell surface composition

Cited by 76 publications

References 70 publications

Mycolic acid-containing bacteria trigger distinct types of membrane vesicles through different routes

Mycolic acid-containing bacteria trigger distinct types of membrane vesicles through different routes

Membrane Vesicle Production as a Bacterial Defense Against Stress

Modulating Isoprenoid Biosynthesis Increases Lipooligosaccharides and Restores Acinetobacter baumannii Resistance to Host and Antibiotic Stress

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