Membrane Vesicle Production as a Bacterial Defense Against Stress

Mozaheb, Negar; Mingeot‐Leclercq, Marie‐Paule

doi:10.3389/fmicb.2020.600221

Cited by 69 publications

(75 citation statements)

References 206 publications

(345 reference statements)

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“…In addition to rapid alteration in the phospholipids, Pseudomonads, like all Gram-negative bacteria, use vesiculation as a defence mechanism against various chemical (and non-chemical) stresses [34]. They release outer membrane vesicles (OMVs) with a diameter between 20 and 500 nm into the extracellular space, thereby altering the composition of the lipopolysaccharide (LPS) layer, the most distal part of their bacterial cell envelope.…”

Section: Built-in Cell Envelope Stress Response As Support Of Bioproductionmentioning

confidence: 99%

“…They release outer membrane vesicles (OMVs) with a diameter between 20 and 500 nm into the extracellular space, thereby altering the composition of the lipopolysaccharide (LPS) layer, the most distal part of their bacterial cell envelope. OMV formation and its numerous functions have been reviewed in detail [27,[34][35][36][37]. The fast release of OMVs plays a major role in stress response, leading to a more hydrophobic bacterial surface and thus enhancing biofilm formation [38].…”

Section: Built-in Cell Envelope Stress Response As Support Of Bioproductionmentioning

confidence: 99%

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Towards robust Pseudomonas cell factories to harbour novel biosynthetic pathways

Bitzenhofer

Kruse

Thies

et al. 2021

Essays in Biochemistry

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Biotechnological production in bacteria enables access to numerous valuable chemical compounds. Nowadays, advanced molecular genetic toolsets, enzyme engineering as well as the combinatorial use of biocatalysts, pathways, and circuits even bring new-to-nature compounds within reach. However, the associated substrates and biosynthetic products often cause severe chemical stress to the bacterial hosts. Species of the Pseudomonas clade thus represent especially valuable chassis as they are endowed with multiple stress response mechanisms, which allow them to cope with a variety of harmful chemicals. A built-in cell envelope stress response enables fast adaptations that sustain membrane integrity under adverse conditions. Further, effective export machineries can prevent intracellular accumulation of diverse harmful compounds. Finally, toxic chemicals such as reactive aldehydes can be eliminated by oxidation and stress-induced damage can be recovered. Exploiting and engineering these features will be essential to support an effective production of natural compounds and new chemicals. In this article, we therefore discuss major resistance strategies of Pseudomonads along with approaches pursued for their targeted exploitation and engineering in a biotechnological context. We further highlight strategies for the identification of yet unknown tolerance-associated genes and their utilisation for engineering next-generation chassis and finally discuss effective measures for pathway fine-tuning to establish stable cell factories for the effective production of natural compounds and novel biochemicals.

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Section: Built-in Cell Envelope Stress Response As Support Of Bioproductionmentioning

confidence: 99%

Section: Built-in Cell Envelope Stress Response As Support Of Bioproductionmentioning

confidence: 99%

Towards robust Pseudomonas cell factories to harbour novel biosynthetic pathways

Bitzenhofer

Kruse

Thies

et al. 2021

Essays in Biochemistry

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“…Membranes vesicles have been observed in D. alaskensis DSM16109, in cultures incubated in presence or absence of mitomycin C [93]. A previous study has suggested that after peptidoglycan lysis caused by endolysins, membrane vesicles can be formed from membranes [94]. Afterwards, in the present study we attempted to test cross infection among the three strains.…”

Section: Induction Of Desulfovibrio Prophagesmentioning

confidence: 76%

Ecophysiological Features Shape the Distribution of Prophages and CRISPR in Sulfate Reducing Prokaryotes

et al. 2021

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Sulfate reducing prokaryotes (SRP) are a phylogenetically and physiologically diverse group of microorganisms that use sulfate as an electron acceptor. SRP have long been recognized as key players of the carbon and sulfur cycles, and more recently, they have been identified to play a relevant role as part of syntrophic and symbiotic relations and the human microbiome. Despite their environmental relevance, there is a poor understanding about the prevalence of prophages and CRISPR arrays and how their distribution and dynamic affect the ecological role of SRP. We addressed this question by analyzing the results of a comprehensive survey of prophages and CRISPR in a total of 91 genomes of SRP with several genotypic, phenotypic, and physiological traits, including genome size, cell volume, minimum doubling time, cell wall, and habitat, among others. Our analysis discovered 81 prophages in 51 strains, representing the 56% of the total evaluated strains. Prophages are non-uniformly distributed across the SRP phylogeny, where prophage-rich lineages belonged to Desulfovibrionaceae and Peptococcaceae. Furthermore, our study found 160 CRISPR arrays in 71 SRP, which is more abundant and widely spread than previously expected. Although there is no correlation between presence and abundance of prophages and CRISPR arrays at the strain level, our analysis showed that there is a directly proportional relation between cellular volumes and number of prophages per cell. This result suggests that there is an additional selective pressure for strains with smaller cells to get rid of foreign DNA, such as prophages, but not CRISPR, due to less availability of cellular resources. Analysis of the prophage genes encoding viral structural proteins reported that 44% of SRP prophages are classified as Myoviridae, and comparative analysis showed high level of homology, but not synteny, among prophages belonging to the Family Desulfovibrionaceae. We further recovered viral-like particles and structures that resemble outer membrane vesicles from D. vulgaris str. Hildenborough. The results of this study improved the current understanding of dynamic interactions between prophages and CRISPR with their hosts in both cultured and hitherto-uncultured SRP strains, and how their distribution affects the microbial community dynamics in several sulfidogenic natural and engineered environments.

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“…In addition, they have great potential in immunology and biotechnology applications. For these reasons in recent years, numerous studies have investigated and reviewed all the aspects of bacterial MVs, including their composition, functions, biogenesis mechanisms, immunomodulatory capacity, and potential applications (Mashburn-Warren and Whiteley, 2006;Schooling and Beveridge, 2006;Lee et al, 2008;Kaparakis-Liaskos and Ferrero, 2015;Schwechheimer and Kuehn, 2015;Jan, 2017;Mozaheb and Mingeot-Leclercq, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…These new types of vesicles are also found to be secreted by pathogenic Gram-negative bacteria (Pérez-Cruz et al, 2015). Although the roles played by stress factors such as antibiotics and environmental growth conditions in promoting vesiculation in many bacteria are already known (Mozaheb and Mingeot-Leclercq, 2020), no stress factors have been identified that help to produce blebbing O-IMVs in S. vesiculosa M7 T .…”

Section: Introductionmentioning

confidence: 99%

Phage-Mediated Explosive Cell Lysis Induces the Formation of a Different Type of O-IMV in Shewanella vesiculosa M7T

et al. 2021

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Shewanella vesiculosa M7T is a cold-adapted Antarctic bacterium that has a great capacity to secrete membrane vesicles (MVs), making it a potentially excellent model for studying the vesiculation process. S. vesiculosa M7T undergoes a blebbing mechanism to produce different types of MVs, including outer membrane vesicles and outer-inner membrane vesicles (O-IMVs). More recently, other mechanisms have been considered that could lead to the formation of O-IMVs derived from prophage-mediated explosive cell lysis in other bacteria, but it is not clear if they are of the same type. The bacterial growth phase could also have a great impact on the type of MVs, although there are few studies on the subject. In this study, we used high-resolution flow cytometry, transmission electron microscopy, and cryo-electron microscopy (Cryo-EM) analysis to determine the amount and types of MVs S. vesiculosa M7T secreted during different growth phases. We show that MV secretion increases during the transition from the late exponential to the stationary phase. Moreover, prophage-mediated explosive cell lysis is activated in S. vesiculosa M7T, increasing the heterogeneity of both single- and double-layer MVs. The sequenced DNA fragments from the MVs covered the entire genome, confirming this explosive cell lysis mechanism. A different structure and biogenesis mechanisms for the explosive cell lysis-derived double-layered MVs was observed, and we propose to name them explosive O-IMVs, distinguishing them from the blebbing O-IMVs; their separation is a first step to elucidate their different functions. In our study, we used for the first time sorting by flow cytometry and Cryo-EM analyses to isolate bacterial MVs based on their nucleic acid content. Further improvements and implementation of bacterial MV separation techniques is essential to develop more in-depth knowledge of MVs.

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Membrane Vesicle Production as a Bacterial Defense Against Stress

Cited by 69 publications

References 206 publications

Towards robust Pseudomonas cell factories to harbour novel biosynthetic pathways

Towards robust Pseudomonas cell factories to harbour novel biosynthetic pathways

Ecophysiological Features Shape the Distribution of Prophages and CRISPR in Sulfate Reducing Prokaryotes

Phage-Mediated Explosive Cell Lysis Induces the Formation of a Different Type of O-IMV in Shewanella vesiculosa M7T

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