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Membrane Vesicle Production As a Bacterial Defense Against Stress

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Membrane Vesicle Production As a Bacterial Defense Against Stress fmicb-11-600221 December 3, 2020 Time: 17:26 # 1 REVIEW published: 09 December 2020 doi: 10.3389/fmicb.2020.600221 Membrane Vesicle Production as a Bacterial Defense Against Stress Negar Mozaheb and Marie-Paule Mingeot-Leclercq* Université catholique de Louvain (UCL), Louvain Drug Research Institute (LDRI), Cellular & Molecular Pharmacology Unit (FACM), Brussels, Belgium 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 Edited by: types of antibacterial treatments. Additionally, membrane vesicles can also provide Hauke Smidt, benefits for the wider bacterial community during infections, through the transfer of Wageningen University and Research, Netherlands resistance or virulence factors. Hence, given that membrane vesicle production may Reviewed by: affect the activities of antibacterial agents, their production should be considered when Armen Trchounian, administering antibacterial treatments. Besides, regarding that membrane vesicles play Yerevan State University, Armenia Yosuke Tashiro, vital roles in bacteria, disrupting their production may suggest an alternative strategy Shizuoka University, Japan for battling against pathogens. Here, we aim to review the stressors encountered by *Correspondence: pathogens and shed light on the roles of membrane vesicles in increasing pathogen Marie-Paule Mingeot-Leclercq adaptabilities in the presence of stress-inducing factors. [email protected] Keywords: pathogen, antibiotics, membrane, environmental stress, membrane vesiculation Specialty section: This article was submitted to Microbial Physiology and Metabolism, INTRODUCTION a section of the journal Frontiers in Microbiology Bacterial membrane vesicles are membrane-derived vesicles discharged by both Gram-positive Received: 01 September 2020 and Gram-negative bacteria. They are heterogeneous in terms of their origin, components, and Accepted: 16 November 2020 size. Vesicles derived from Gram-positive bacteria are 20–400 nm in size, while those derived Published: 09 December 2020 from Gram-negative bacteria are 20–200 nm (Schwechheimer and Kuehn, 2015; Toyofuku et al., Citation: 2017). Membrane vesicles are promising vaccine and adjuvant candidates (Ellis and Kuehn, 2010; Mozaheb N and Jan, 2017). Nonetheless, their production should be strictly controlled when dealing with bacterial Mingeot-Leclercq M-P (2020) Membrane Vesicle Production as infections, primarily because membrane vesicles exert highly deleterious effects on the effectiveness a Bacterial Defense Against Stress. of various antimicrobial agents, intensify the consequences of infections, and are also virulence Front. Microbiol. 11:600221. factors for bacteria (MacDonald and Kuehn, 2012; Chattopadhyay and Jagannadham, 2015; doi: 10.3389/fmicb.2020.600221 Devos et al., 2017). Frontiers in Microbiology| www.frontiersin.org 1 December 2020| Volume 11| Article 600221 fmicb-11-600221 December 3, 2020 Time: 17:26 # 2 Mozaheb and Mingeot-Leclercq Bacterial Vesiculation Against Stress Numerous excellent reviews have been published regarding Outer membrane blebbing is accompanied by turnover of the the various functions and characteristics of bacterial membrane outer membrane, and it resulted in production of OMVs vesicles. For instance, Toyofuku et al.(2019) classified membrane containing LPS, and some vesicles have components of the vesicles into four distinct types depending on their origin, inner membrane as well. Cytoplasmic turgor pressure can lead biogenesis pathway, contents, and functions. Moreover, to the formation of outer–inner membrane vesicles (OIMVs) several studies on factors that trigger the production of (Toyofuku et al., 2019). membrane vesicles in Gram-negative bacteria have allowed Membrane vesicles released after explosive lysis are formed the categorization of these factors, and suggested various from broken membrane fractions that have reassembled while vesiculation models in Gram-negative bacteria (Schwechheimer retaining some cytoplasmic material and periplasm. Induction and Kuehn, 2015). Given that membrane vesicle production of endogenous bacterial hydrolases or treatment with an agent is conserved among bacteria, and that they have a prominent that disrupts peptidoglycan synthesis can result in explosive cell role in transporting cellular contents, membrane vesicles have lysis (Li et al., 1996; Kawai et al., 2018) and membrane vesicle been called the type zero secretion system (Guerrero-Mandujano formation; this has been observed in both Gram-negative and et al., 2017). Membrane vesicles are mediators of bacterial -positive cells (Turnbull et al., 2016; Toyofuku et al., 2017). interspecies and cross-species communication, as well as In the latter, membrane vesiculation may be triggered by an effective mediators of host–microbe interactions, which helps increase in cytoplasmic turgor and/or at a weakened point in bacteria with colonization and dispersal (Caruana and Walper, the peptidoglycan layer of the cell wall, through which the 2020). A significant number of studies have also investigated the cytoplasmic membrane and part of cytoplasm pass to form contribution of membrane vesicles produced by both pathogens membrane vesicles (Brown et al., 2015). Such vesiculation and commensals in modulating host immune system responses often leads to cell death and is referred to as bubbling cell (Ellis and Kuehn, 2010; Kaparakis-Liaskos and Ferrero, 2015). death (Toyofuku et al., 2019). Although there are mechanistic differences between bubbling cell death and vesiculation in Gram-positive bacteria caused by explosive cell lysis, in practice Membrane Vesicles Biogenesis there is no clear distinction between vesicles produced through General Mechanisms the two processes. Evidence indicates that the biogenesis of outer membrane vesicles (OMVs) in Gram-negative bacteria relies on four main Role of Inner Membrane for OMV Production mechanisms: (i) dissociation of the outer membrane in specific Studies based on stochastic as well as non-stochastic models zones lacking proper attachments to underlying structures (e.g., of membrane vesiculation have shown that it is a highly peptidoglycans) (Yeh et al., 2010; Moon et al., 2012); (ii) the regulated process. Most studies to date on membrane vesiculation presence of misfolded proteins, which accumulate in nano- have focused on Gram-negative bacteria (and hence, OMVs). domains where crosslinks between peptidoglycans and other However, recently there has been increasing interest in the components of the bacterial envelope are either locally depleted regulatory role of the inner membrane (Davies et al., 2019; or displaced (Schwechheimer and Kuehn, 2015); (iii) changes in Takaki et al., 2020). The role of inner membrane in outer lipopolysaccharide (LPS) structure which presumably results in membrane vesiculation could be considered via various aspects, the generation of a differential curvature, fluidity, and charge in including (I) Inner membrane regulates and keeps the cross- the outer membrane (Elhenawy et al., 2016; Volgers et al., 2018); talk between the components of the bacterial envelope, e.g., and (iv) disruption of the maintenance of lipid asymmetry in outer membrane-peptidoglycan-inner membrane, (II) Inner the outer membrane, based on presence of phospholipids in the membrane regulates the stress response-pathway, (III) Inner outer leaflet of the outer membrane. Figure 1 depicts the origins membrane contains maintenance elements for outer membrane and mechanistic reasons for membrane vesiculation. The factors asymmetry (IV) Inner membrane can convey the turgor pressure underlying the promotion of membrane vesicle production in of misfolded proteins and SOS response-pathway to periplasm Gram-positive may be similar to those in Gram-negative bacteria, and outer membrane. The following paragraphs present the with membrane vesicles reflecting stress-induced membrane explanation of each role. remodeling (Nagakubo et al., 2019). Although a variety of (I) Inner membrane and envelope integrity. Correct models have been proposed for membrane vesicle production localization of lipoproteins is critical for their function and in Gram-negative bacteria, relatively few models have been depends on efficient modification and transport as well as suggested for Gram-positive bacteria (Brown et al., 2015; accurate sorting of lipoproteins. All lipoproteins are translated Resch et al., 2016). in the cytoplasm as preprolipoprotein precursor proteins. After According to conventional models, membrane vesiculation their export through the cytoplasmic membrane, which occurs does not involve cell lysis or death. As this is not supported by predominantly but not exclusively via the general secretory
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