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      Extracellular membrane vesicles in the three domains of life and beyond

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          Abstract

          Cells from all three domains of life, Archaea, Bacteria and Eukarya, produce extracellular vesicles (EVs) which are sometimes associated with filamentous structures known as nanopods or nanotubes. The mechanisms of EV biogenesis in the three domains remain poorly understood, although studies in Bacteria and Eukarya indicate that the regulation of lipid composition plays a major role in initiating membrane curvature. EVs are increasingly recognized as important mediators of intercellular communication via transfer of a wide variety of molecular cargoes. They have been implicated in many aspects of cell physiology such as stress response, intercellular competition, lateral gene transfer (via RNA or DNA), pathogenicity and detoxification. Their role in various human pathologies and aging has aroused much interest in recent years. EVs can be used as decoys against viral attack but virus-infected cells also produce EVs that boost viral infection. Here, we review current knowledge on EVs in the three domains of life and their interactions with the viral world.

          Abstract

          This review discusses the current research on extracellular vesicle (EV) biology and their various roles in the three domains of life: Archaea, Bacteria and Eukarya. The physiological and/or evolutionary relationships between EVs and viruses are also examined.

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          Most cited references258

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          Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.

          Molecular structures and sequences are generally more revealing of evolutionary relationships than are classical phenotypes (particularly so among microorganisms). Consequently, the basis for the definition of taxa has progressively shifted from the organismal to the cellular to the molecular level. Molecular comparisons show that life on this planet divides into three primary groupings, commonly known as the eubacteria, the archaebacteria, and the eukaryotes. The three are very dissimilar, the differences that separate them being of a more profound nature than the differences that separate typical kingdoms, such as animals and plants. Unfortunately, neither of the conventionally accepted views of the natural relationships among living systems--i.e., the five-kingdom taxonomy or the eukaryote-prokaryote dichotomy--reflects this primary tripartite division of the living world. To remedy this situation we propose that a formal system of organisms be established in which above the level of kingdom there exists a new taxon called a "domain." Life on this planet would then be seen as comprising three domains, the Bacteria, the Archaea, and the Eucarya, each containing two or more kingdoms. (The Eucarya, for example, contain Animalia, Plantae, Fungi, and a number of others yet to be defined). Although taxonomic structure within the Bacteria and Eucarya is not treated herein, Archaea is formally subdivided into the two kingdoms Euryarchaeota (encompassing the methanogens and their phenotypically diverse relatives) and Crenarchaeota (comprising the relatively tight clustering of extremely thermophilic archaebacteria, whose general phenotype appears to resemble most the ancestral phenotype of the Archaea.
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            Biogenesis and secretion of exosomes.

            Although observed for several decades, the release of membrane-enclosed vesicles by cells into their surrounding environment has been the subject of increasing interest in the past few years, which led to the creation, in 2012, of a scientific society dedicated to the subject: the International Society for Extracellular Vesicles. Convincing evidence that vesicles allow exchange of complex information fuelled this rise in interest. But it has also become clear that different types of secreted vesicles co-exist, with different intracellular origins and modes of formation, and thus probably different compositions and functions. Exosomes are one sub-type of secreted vesicles. They form inside eukaryotic cells in multivesicular compartments, and are secreted when these compartments fuse with the plasma membrane. Interestingly, different families of molecules have been shown to allow intracellular formation of exosomes and their subsequent secretion, which suggests that even among exosomes different sub-types exist. Copyright © 2014 Elsevier Ltd. All rights reserved.
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              Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes

              Some pathogens and pests deliver small RNAs (sRNAs) into host cells to suppress host immunity. Conversely, hosts also transfer sRNAs into pathogens and pests to inhibit their virulence. Although sRNA trafficking has been observed in a wide variety of interactions, how sRNAs are transferred, especially from hosts to pathogens/pests, is still unknown. Here we show that host Arabidopsis cells secrete exosome-like extracellular vesicles to deliver sRNAs into fungal pathogen Botrytis cinerea. These sRNA-containing vesicles accumulate at the infection sites and are taken up by the fungal cells. Transferred host sRNAs induce silencing of fungal genes critical for pathogenicity. Thus, Arabidopsis has adapted exosome-mediated cross-kingdom RNA interference as part of its immune responses during the evolutionary arms race with the pathogen.
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                Author and article information

                Journal
                FEMS Microbiol Rev
                FEMS Microbiol. Rev
                femsre
                FEMS Microbiology Reviews
                Oxford University Press
                0168-6445
                1574-6976
                21 November 2018
                May 2019
                21 November 2018
                : 43
                : 3
                : 273-303
                Affiliations
                [1 ]Institute for Integrative Biology of the Cell (I2BC), Biologie Cellulaire des Archées (BCA), CEA, CNRS, Université Paris-Sud, 91405 Orsay cedex, France
                [2 ]Institut Pasteur, Unité de Biologie Moléculaire du Gène chez les Extrêmophiles, Département de Microbiologie, F75015 Paris, France
                Author notes
                Corresponding author: Unité de Biologie Moléculaire du Gène chez les Extrêmophiles (BMGE), Département de Microbiologie, Institut Pasteur, 25 Rue du Docteur Roux, 75015 Paris, France. Tel: +33145688791; E-mail: patrick.forterre@ 123456pasteur.fr
                Article
                fuy042
                10.1093/femsre/fuy042
                6524685
                30476045
                993deba2-3dc4-4590-9577-bdc08245519f
                © FEMS 2018.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 03 August 2017
                : 20 November 2018
                Page count
                Pages: 31
                Funding
                Funded by: Seventh Framework Program
                Award ID: FP7/2007-2013
                Categories
                Review Article

                Microbiology & Virology
                extracellular vesicles,nanotubes,archaea,virus,evolution,luca
                Microbiology & Virology
                extracellular vesicles, nanotubes, archaea, virus, evolution, luca

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