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Tracing the Archaeal Origins of Eukaryotic Membrane-Trafficking System Building Blocks
Univ Alberta, Dept Cell Biol, Edmonton, AB, Canada..
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Univ Alberta, Dept Cell Biol, Edmonton, AB, Canada..
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
2016 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 33, no 6, 1528-1541 p.Article in journal (Refereed) PublishedText
Abstract [en]

In contrast to prokaryotes, eukaryotic cells are characterized by a complex set of internal membrane-bound compartments. A subset of these, and the protein machineries that move material between them, define the membrane-trafficking system (MTS), the emergence of which represents a landmark in eukaryotic evolution. Unlike mitochondria and plastids, MTS organelles have autogenous origins. Much of the MTS machinery is composed of building blocks, including small GTPase, coiled-coil, beta-propeller + alpha-solenoid, and longin domains. Despite the identification of prokaryotic proteins containing these domains, only few represent direct orthologues, leaving the origins and early evolution of the MTS poorly understood. Here, we present an in-depth analysis of MTS building block homologues in the composite genome of Lokiarchaeum, the recently discovered archaeal sister clade of eukaryotes, yielding several key insights. We identify two previously unreported Eukaryotic Signature Proteins; orthologues of the Gtr/Rag family GTPases, involved in target of rapamycin complex signaling, and of the RLC7 dynein component. We could not identify golgin or SNARE (coiled-coil) or beta-propeller + alpha-solenoid orthologues, nor typical MTS domain fusions, suggesting that these either were lost from Lokiarchaeum or emerged later in eukaryotic evolution. Furthermore, our phylogenetic analyses of lokiarchaeal GTPases support a split into Ras-like and Arf-like superfamilies, with different prokaryotic antecedents, before the advent of eukaryotes. While no GTPase activating proteins or exchange factors were identified, we show that Lokiarchaeum encodes numerous roadblock domain proteins and putative longin domain proteins, confirming the latter's origin from Archaea. Altogether, our study provides new insights into the emergence and early evolution of the eukaryotic membrane-trafficking system.

Place, publisher, year, edition, pages
2016. Vol. 33, no 6, 1528-1541 p.
Keyword [en]
archaea, eukaryogenesis, longin domain, membrane trafficking, roadblock domain, small GTPases, Lokiarchaeum
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:uu:diva-298076DOI: 10.1093/molbev/msw034ISI: 000376170300011PubMedID: 26893300OAI: oai:DiVA.org:uu-298076DiVA: diva2:944832
Funder
EU, European Research Council, 310039-PUZZLE_CELLSwedish Foundation for Strategic Research , FFL12-0024
Available from: 2016-06-30 Created: 2016-06-29 Last updated: 2016-06-30Bibliographically approved

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Spang, AnjaEttema, Thijs J. G.
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