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      Origin and evolution of metabolic sub-cellular compartmentalization in eukaryotes

      review-article
      a , b , c , , a , b
      Biochimie
      Editions Scientifiques Elsevier
      Evolution, Eukaryotes, Compartments, Organelles

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          Abstract

          A high level of subcellular compartmentalization is a hallmark of eukaryotic cells. This intricate internal organization was present already in the common ancestor of all extant eukaryotes, and the determination of the origins and early evolution of the different organelles remains largely elusive. Organellar proteomes are determined through regulated pathways that target proteins produced in the cytosol to their final subcellular destinations. This internal sorting of proteins can vary across different physiological conditions, cell types and lineages. Evolutionary retargeting – the alteration of a subcellular localization of a protein in the course of evolution – has been rampant in eukaryotes and involves any possible combination of organelles. This fact adds another layer of difficulty to the reconstruction of the origins and evolution of organelles. In this review we discuss current themes in relation to the origin and evolution of organellar proteomes. Throughout the text, a special focus is set on the evolution of mitochondrial and peroxisomal proteomes, which are two organelles for which extensive proteomic and evolutionary studies have been performed.

          Highlights

          • Eukaryotes have a complex subcellular organization.

          • This feature is ancestral and the origin of most compartments remains unknown.

          • Subcellular retargeting of proteins have been rampant during evolution.

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          Most cited references51

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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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            Mitochondrial evolution.

            The serial endosymbiosis theory is a favored model for explaining the origin of mitochondria, a defining event in the evolution of eukaryotic cells. As usually described, this theory posits that mitochondria are the direct descendants of a bacterial endosymbiont that became established at an early stage in a nucleus-containing (but amitochondriate) host cell. Gene sequence data strongly support a monophyletic origin of the mitochondrion from a eubacterial ancestor shared with a subgroup of the alpha-Proteobacteria. However, recent studies of unicellular eukaryotes (protists), some of them little known, have provided insights that challenge the traditional serial endosymbiosis-based view of how the eukaryotic cell and its mitochondrion came to be. These data indicate that the mitochondrion arose in a common ancestor of all extant eukaryotes and raise the possibility that this organelle originated at essentially the same time as the nuclear component of the eukaryotic cell rather than in a separate, subsequent event.
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              Magnetosome formation in prokaryotes.

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                Author and article information

                Contributors
                Journal
                Biochimie
                Biochimie
                Biochimie
                Editions Scientifiques Elsevier
                0300-9084
                1638-6183
                1 December 2015
                December 2015
                : 119
                : 262-268
                Affiliations
                [a ]Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader, 88, 08003 Barcelona, Spain
                [b ]Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain
                [c ]Institució Catalana de Recerca i Estudis Avançats (ICREA), Pg. Lluís Companys 23, 08010 Barcelona, Spain
                Author notes
                []Corresponding author. Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader, 88, 08003 Barcelona, Spain. tgabaldon@ 123456crg.es
                Article
                S0300-9084(15)00090-5
                10.1016/j.biochi.2015.03.021
                4678951
                25869000
                788e73c7-07a4-4878-9a0b-5c816debbe3a
                © 2015 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 6 February 2015
                : 25 March 2015
                Categories
                Mini-Review

                Biochemistry
                evolution,eukaryotes,compartments,organelles
                Biochemistry
                evolution, eukaryotes, compartments, organelles

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