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      Delayed cytokinesis generates multinuclearity and potential advantages in the amoeba Acanthamoeba castellanii Neff strain

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          Abstract

          Multinuclearity is a widespread phenomenon across the living world, yet how it is achieved, and the potential related advantages, are not systematically understood. In this study, we investigate multinuclearity in amoebae. We observe that non-adherent amoebae are giant multinucleate cells compared to adherent ones. The cells solve their multinuclearity by a stretchy cytokinesis process with cytosolic bridge formation when adherence resumes. After initial adhesion to a new substrate, the progeny of the multinucleate cells is more numerous than the sibling cells generated from uninucleate amoebae. Hence, multinucleate amoebae show an advantage for population growth when the number of cells is quantified over time. Multiple nuclei per cell are observed in different amoeba species, and the lack of adhesion induces multinuclearity in diverse protists such as Acanthamoeba castellanii, Vermamoeba vermiformis, Naegleria gruberi and Hartmannella rhysodes. In this study, we observe that agitation induces a cytokinesis delay, which promotes multinuclearity. Hence, we propose the hypothesis that multinuclearity represents a physiological adaptation under non-adherent conditions that can lead to biologically relevant advantages.

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          Most cited references18

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          Microorganisms resistant to free-living amoebae.

          Free-living amoebae feed on bacteria, fungi, and algae. However, some microorganisms have evolved to become resistant to these protists. These amoeba-resistant microorganisms include established pathogens, such as Cryptococcus neoformans, Legionella spp., Chlamydophila pneumoniae, Mycobacterium avium, Listeria monocytogenes, Pseudomonas aeruginosa, and Francisella tularensis, and emerging pathogens, such as Bosea spp., Simkania negevensis, Parachlamydia acanthamoebae, and Legionella-like amoebal pathogens. Some of these amoeba-resistant bacteria (ARB) are lytic for their amoebal host, while others are considered endosymbionts, since a stable host-parasite ratio is maintained. Free-living amoebae represent an important reservoir of ARB and may, while encysted, protect the internalized bacteria from chlorine and other biocides. Free-living amoebae may act as a Trojan horse, bringing hidden ARB within the human "Troy," and may produce vesicles filled with ARB, increasing their transmission potential. Free-living amoebae may also play a role in the selection of virulence traits and in adaptation to survival in macrophages. Thus, intra-amoebal growth was found to enhance virulence, and similar mechanisms seem to be implicated in the survival of ARB in response to both amoebae and macrophages. Moreover, free-living amoebae represent a useful tool for the culture of some intracellular bacteria and new bacterial species that might be potential emerging pathogens.
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            Enteropathogens and chronic illness in returning travelers.

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              THE FINE STRUCTURE OF ACANTHAMOEBA CASTELLANII (NEFF STRAIN)

              Encysting cells of Acanthamoeba castellanii, Neff strain, have been examined with the electron microscope. The wall structure and cytoplasmic changes during encystment are described. The cyst wall is composed of two major layers: a laminar, fibrous exocyst with a variable amount of matrix material, and an endocyst of fine fibrils in a granular matrix. The two layers are normally separated by a space except where they form opercula in the center of ostioles (exits for excysting amebae). An additional amorphous layer is probably present between the wall and the protoplast in the mature cyst. Early in encystment the Golgi complex is enlarged and contains a densely staining material that appears to contribute to wall formation. Vacuoles containing cytoplasmic debris (autolysosomes) are present in encysting cells and the contents of some of the vacuoles are deposited in the developing cyst wall. Lamellate bodies develop in the mitochondria and appear in the cytoplasm. Several changes are associated with the mitochondrial intracristate granule. The nucleus releases small buds into the cytoplasm, and the nucleolus decreases to less than half its original volume. The cytoplasm increases in electron density and its volume is reduced by about 80%. The water expulsion vesicle is the only cellular compartment without dense content in the mature cyst. The volume fractions of lipid droplets, Golgi complex, mitochondria, digestive vacuoles, and autolysosomes have been determined at different stages of encystment by stereological analysis of electron micrographs. By chemical analyses, dry weight, protein, phospholipid, and glycogen are lower and neutral lipid is higher in the mature cyst than in the trophozoite.
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                Author and article information

                Contributors
                charles.vanderhenst@vub.vib.be
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                21 July 2020
                21 July 2020
                2020
                : 10
                : 12109
                Affiliations
                [1 ]ISNI 0000 0001 2242 8479, GRID grid.6520.1, Laboratory of Evolutionary Genetics and Ecology, , URBE, University of Namur, ; Namur, Belgium
                [2 ]ISNI 0000 0001 2160 6368, GRID grid.11166.31, Laboratoire Ecologie et Biologie des Interactions, Equipe Microbiologie de L’Eau, , Université de Poitiers, UMR CNRS 7267, ; 86073 Poitiers, France
                [3 ]ISNI 0000 0001 2242 8479, GRID grid.6520.1, Research Unit in the Biology of Microorganisms (URBM), , NARILIS, University of Namur (UNamur), ; Namur, Belgium
                [4 ]ISNI 0000 0001 2290 8069, GRID grid.8767.e, Microbial Resistance and Drug Discovery, Center for Structural Biology (CSB), Flanders Institute for Biotechnology (VIB), , Vrije Universiteit Brussel (VUB), ; Pleinlaan 2, Building E-3, 1050 Brussels, Belgium
                [5 ]ISNI 0000 0001 2290 8069, GRID grid.8767.e, Structural Biology Brussels, , Vrije Universiteit Brussel (VUB), ; Brussels, Belgium
                Article
                68694
                10.1038/s41598-020-68694-9
                7374626
                32694508
                d03490d6-f40d-437a-97a3-3cb9a01112a0
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 10 March 2020
                : 26 June 2020
                Categories
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                Custom metadata
                © The Author(s) 2020

                Uncategorized
                parasitology,evolutionary ecology,microbial ecology
                Uncategorized
                parasitology, evolutionary ecology, microbial ecology

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