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On the Archaeal Origins of Eukaryotes and the Challenges of Inferring Phenotype from Genotype

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      Abstract

      If eukaryotes arose through a merger between archaea and bacteria, what did the first true eukaryotic cell look like? A major step toward an answer came with the discovery of Lokiarchaeum, an archaeon whose genome encodes small GTPases related to those used by eukaryotes to regulate membrane traffic. Although ‘Loki’ cells have yet to be seen, their existence has prompted the suggestion that the archaeal ancestor of eukaryotes engulfed the future mitochondrion by phagocytosis. We propose instead that the archaeal ancestor was a relatively simple cell, and that eukaryotic cellular organization arose as the result of a gradual transfer of bacterial genes and membranes driven by an ever-closer symbiotic partnership between a bacterium and an archaeon.

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      Eukaryotes are thought to be a product of symbiosis between archaea and bacteria. The recently discovered Lokiarchaeum (‘Loki’) encodes more Eukaryotic Signature Proteins (ESPs) than any other archaeon, making it the closest living relative to the putative ancestor of eukaryotes.Lokiarchaeum is the first prokaryote found to encode small GTPases, gelsolin, BAR domains, and longin domains, leading many to suggest that it might be compartmentalized and be capable of membrane trafficking.Many models for the evolution of eukaryotes invoke an archaeal ancestor that is capable of phagocytosis to explain the entry of the future mitochondrion into the host cell.Understanding the cell biology of Lokiarchaeum will be key to understanding the morphological transitions that characterized the evolution of eukaryotic cellular architecture, but Loki has not yet been cultured or seen.

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      Most cited references 78

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      Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids.

      The mTORC1 kinase promotes growth in response to growth factors, energy levels, and amino acids, and its activity is often deregulated in disease. The Rag GTPases interact with mTORC1 and are proposed to activate it in response to amino acids by promoting mTORC1 translocation to a membrane-bound compartment that contains the mTORC1 activator, Rheb. We show that amino acids induce the movement of mTORC1 to lysosomal membranes, where the Rag proteins reside. A complex encoded by the MAPKSP1, ROBLD3, and c11orf59 genes, which we term Ragulator, interacts with the Rag GTPases, recruits them to lysosomes, and is essential for mTORC1 activation. Constitutive targeting of mTORC1 to the lysosomal surface is sufficient to render the mTORC1 pathway amino acid insensitive and independent of Rag and Ragulator, but not Rheb, function. Thus, Rag-Ragulator-mediated translocation of mTORC1 to lysosomal membranes is the key event in amino acid signaling to mTORC1. Copyright 2010 Elsevier Inc. All rights reserved.
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        Horizontal gene transfer in prokaryotes: quantification and classification.

        Comparative analysis of bacterial, archaeal, and eukaryotic genomes indicates that a significant fraction of the genes in the prokaryotic genomes have been subject to horizontal transfer. In some cases, the amount and source of horizontal gene transfer can be linked to an organism's lifestyle. For example, bacterial hyperthermophiles seem to have exchanged genes with archaea to a greater extent than other bacteria, whereas transfer of certain classes of eukaryotic genes is most common in parasitic and symbiotic bacteria. Horizontal transfer events can be classified into distinct categories of acquisition of new genes, acquisition of paralogs of existing genes, and xenologous gene displacement whereby a gene is displaced by a horizontally transferred ortholog from another lineage (xenolog). Each of these types of horizontal gene transfer is common among prokaryotes, but their relative contributions differ in different lineages. The fixation and long-term persistence of horizontally transferred genes suggests that they confer a selective advantage on the recipient organism. In most cases, the nature of this advantage remains unclear, but detailed examination of several cases of acquisition of eukaryotic genes by bacteria seems to reveal the evolutionary forces involved. Examples include isoleucyl-tRNA synthetases whose acquisition from eukaryotes by several bacteria is linked to antibiotic resistance, ATP/ADP translocases acquired by intracellular parasitic bacteria, Chlamydia and Rickettsia, apparently from plants, and proteases that may be implicated in chlamydial pathogenesis.
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          ARF proteins: roles in membrane traffic and beyond.

          The ADP-ribosylation factor (ARF) small GTPases regulate vesicular traffic and organelle structure by recruiting coat proteins, regulating phospholipid metabolism and modulating the structure of actin at membrane surfaces. Recent advances in our understanding of the signalling pathways that are regulated by ARF1 and ARF6, two of the best characterized ARF proteins, provide a molecular context for ARF protein function in fundamental biological processes, such as secretion, endocytosis, phagocytosis, cytokinesis, cell adhesion and tumour-cell invasion.
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            Author and article information

            Affiliations
            [1 ]MRC Laboratory for Molecular Cell Biology, University College London, Gower Street, London WC1E 6BT, UK
            [2 ]National Centre for Biological Sciences, TIFR, GKVK, Bellary Road, Bengaluru 560065, India
            Author notes
            Contributors
            Journal
            Trends Cell Biol
            Trends Cell Biol
            Trends in Cell Biology
            Elsevier Science Publishers
            0962-8924
            1879-3088
            1 July 2016
            July 2016
            : 26
            : 7
            : 476-485
            27319280
            4917890
            S0962-8924(16)30002-2
            10.1016/j.tcb.2016.03.009
            © 2016 The Authors

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

            Categories
            Opinion
            Special Issue: 25 Years of Trends in Cell Biology

            Cell biology

            lokiarchaeum, gtpase, evolution, eukaryogenesis

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