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Cited by 268Origins and Evolution of LifeProtist diversity and phylogenyGenomics and Phylogenetic Studies

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The Last Universal Common Ancestor: emergence, constitution and genetic legacy of an elusive forerunner

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Glansdorff, Nicolas, Xu, Ying, Labedan, Bernard·2008·Biology Direct
DOI 10.1186/1745-6150-3-29PMC PMC2478661
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Abstract

Background: Since the reclassification of all life forms in three Domains (Archaea, Bacteria, Eukarya), the identity of their alleged forerunner (Last Universal Common Ancestor or LUCA) has been the subject of extensive controversies: progenote or already complex organism, prokaryote or protoeukaryote, thermophile or mesophile, product of a protracted progression from simple replicators to complex cells or born in the cradle of "catalytically closed" entities? We present a critical survey of the topic and suggest a scenario. Results: LUCA does not appear to have been a simple, primitive, hyperthermophilic prokaryote but rather a complex community of protoeukaryotes with a RNA genome, adapted to a broad range of moderate temperatures, genetically redundant, morphologically and metabolically diverse. LUCA's genetic redundancy predicts loss of paralogous gene copies in divergent lineages to be a significant source of phylogenetic anomalies, i.e. instances where a protein tree departs from the SSU-rRNA genealogy; consequently, horizontal gene transfer may not have the rampant character assumed by many. Examining membrane lipids suggest LUCA had sn1,2 ester fatty acid lipids from which Archaea emerged from the outset as thermophilic by "thermoreduction," with a new type of membrane, composed of sn2,3 ether isoprenoid lipids; this occurred without major enzymatic reconversion. Bacteria emerged by reductive evolution from LUCA and some lineages further acquired extreme thermophily by convergent evolution. This scenario is compatible with the hypothesis that the RNA to DNA transition resulted from different viral invasions as proposed by Forterre. Beyond the controversy opposing "replication first" to metabolism first", the predictive arguments of theories on "catalytic closure" or "compositional heredity" heavily weigh in favour of LUCA's ancestors having emerged as complex, self-replicating entities from which a genetic code arose under natural selection. Conclusion: Life was born complex and the LUCA displayed that heritage. It had the "body "of a mesophilic eukaryote well before maturing by endosymbiosis into an organism adapted to an atmosphere rich in oxygen. Abundant indications suggest reductive evolution of this complex and heterogeneous entity towards the "prokaryotic" Domains Archaea and Bacteria. The word "prokaryote" should be abandoned because epistemologically unsound. Reviewers: This article was reviewed by Anthony Poole, Patrick Forterre, and Nicolas Galtier.

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Figure 1 Committing steps in the biosynthesis of membrane lipids. The "primary divide" separating Archaea from Bacteria and Eukarya is outlined.
Figure 1 Committing steps in the biosynthesis of membrane lipids. The "primary divide" separating Archaea from Bacteria and Eukarya is outlined.CC BY · PubMed Central
Figure 2 Birth and legacy of the Last Universal Common Ancestor (LUCA). A large, evolving and promiscuous community stretches in time from the origins to the immediate precursors of the three Domains (and perhaps of many other ones, presumably abortive). (A) The "sprouting tuber" analogy [49], illustrated by Juan Miro's "Potato" [Copyright: The Metropolitan Museum of Art, New York, New York, USA. The Potato (1928) by Joan Miró (Spanish, 1893–1983). Oil on canvas; 39 3/4 × 32 1/8 in. (101 × 81.6 cm). Jacques and Natasha Gelman Collection, 1998 (1999.363.50). © 2000 Artists Rights Society (ARS), New York/ADAGP, Paris]; (B) Progression from the inorganic to self-replicating entities via a qualitative jump to complexity by catalytic closure, and further to cells with a DNA genome. The diagram illustrates the proposition that viruses originate from a cellular precursor [45] and that viruses are responsible for the RNA-DNA transition in Bacteria on one side and Archaea/Eukarya on the other [11,12,44]. The exact branching order is not specified (see [44,45] and text). See text for details of the sn1,2→sn2,3 lipids transition. The onset and course of the reductive evolution leading to Archaea or Bacteria are not indicated in detail. We conceive of this process as having occurred in several steps, more a succession of evolutionary crises than a gradual transformation; it involved the emergence of cells with membranes fully competent in electron-transport-driven energy harnessing and the RNA-DNA transition.
Figure 2 Birth and legacy of the Last Universal Common Ancestor (LUCA). A large, evolving and promiscuous community stretches in time from the origins to the immediate precursors of the three Domains (and perhaps of many other ones, presumably abortive). (A) The "sprouting tuber" analogy [49], illustrated by Juan Miro's "Potato" [Copyright: The Metropolitan Museum of Art, New York, New York, USA. The Potato (1928) by Joan Miró (Spanish, 1893–1983). Oil on canvas; 39 3/4 × 32 1/8 in. (101 × 81.6 cm). Jacques and Natasha Gelman Collection, 1998 (1999.363.50). © 2000 Artists Rights Society (ARS), New York/ADAGP, Paris]; (B) Progression from the inorganic to self-replicating entities via a qualitative jump to complexity by catalytic closure, and further to cells with a DNA genome. The diagram illustrates the proposition that viruses originate from a cellular precursor [45] and that viruses are responsible for the RNA-DNA transition in Bacteria on one side and Archaea/Eukarya on the other [11,12,44]. The exact branching order is not specified (see [44,45] and text). See text for details of the sn1,2→sn2,3 lipids transition. The onset and course of the reductive evolution leading to Archaea or Bacteria are not indicated in detail. We conceive of this process as having occurred in several steps, more a succession of evolutionary crises than a gradual transformation; it involved the emergence of cells with membranes fully competent in electron-transport-driven energy harnessing and the RNA-DNA transition.CC BY · PubMed Central

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Research works printed but not linked: 9

  1. Forterre P, Philippe H: Where is the root of the universal tree of life?. Bioessays. 1999, 21: 871-879. 10.1002/(SICI)1521-1878(199910)21:10<871::AID-BIES10>3.0.CO;2-Q. · DOI
  2. Glansdorff N, Xu Y: Phylogeny of extremophiles. Extremophilies in Encyclopedia of Life Support Systems (EOLSS). Edited by: Gerday C, Glansdorff N. 2004, Developed under the Auspicies of the UNESCO, Eolss Publishers, Oxford, UK, [http://www.eolss.net]
  3. Kandler O: The early diversification of life. Nobel Symposium No 84, Early Life on Earth. 1994, Columbia University Press, New York NY, 152-160.
  4. Forterre P: Strategies of extremophily in nucleic acids adaptation to high temperature. Extremophilies in Encyclopedia of Life Support Systems (EOLSS). Edited by: Gerday C, Glansdorff N. 2004, Developed under the auspicies of the UNESCO, Eolss Publishers, Oxford, UK, [http://www.eolss.net]
  5. Glansdorff N, Xu Y: Microbial life at low temperatures: mechanisms of adaptation and extreme biotopes. Implications for exobiology and the origin of life. Recent Res Devel Microbiol. 2002, 6: 1-21.
  6. Sakmann E: Physikalische Grundlagen der molekularen Organisation und Dynamik von Membranen. Biophysik. Edited by: Hoppe W, Lohmann W, Markl H, Ziegler H. 1982, Springer, Berlin, Germany, 439-471. 2
  7. Jensen RA: Evolution of metabolic pathways in enteric bacteria. Escherichia coli and Salmonella: Cellular and Molecular Biology. Edited by: Neidhardt DCFC. Washington: American Society for Microbiology press, 2649-2662.
  8. de Duve C: Blueprint for a Cell. Neil Patterson, Burlington. 1991
  9. Wachtershauser G: Before enzymes and templates. Microbiol Rev. 1988, 52: 452-484. · DOI · Paper page

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Metadata

Authors
Glansdorff, N., Xu, Y., & Labedan, B.
Affiliations
  • Vrije Universiteit Brussel (BE)
  • Université Paris-Sud (FR)
Corresponding author
Labedan, Bernard
ORCID
Venue
Biology Direct
Publisher
Springer Science and Business Media LLC
Published
2008-07-09
Volume
3
Issue
1
Pages
29-29
ISSN
1745-6150 (ISSN-L)
DOI
10.1186/1745-6150-3-29
PMC
PMC2478661
OpenAlex
W2116103056
Cited by
264
References
228
Citations by year
2026: 2 · 2025: 7 · 2024: 10 · 2023: 8 · 2022: 15 · 2021: 17 · 2020: 12 · 2019: 22 · 2018: 12 · 2017: 17 · 2016: 11 · 2015: 16 · 2014: 11 · 2013: 23 · 2012: 10
FWCI
2.73
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Biology Direct (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • VUBIR (Vrije Universiteit Brussel) (submittedVersion)
Funders
  • Agence Nationale de la Recherche (ANR-05)
  • Centre National de la Recherche Scientifique
  • Fondation des Treilles
Topics
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
last universal common ancestor, origin of life, RNA genome, gene redundancy, horizontal gene transfer, membrane lipids, ether lipids, RNA to DNA transition, viral entry, metabolism-first hypothesis, origin of the genetic code
MeSH terms
Archaea, Bacteria, Eukaryotic Cells, Biological Evolution, Phylogeny, Prokaryotic Cells

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