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

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

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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  • LUCA is estimated to have lived 3.8-3.5 billion years ago.

    “LUCA is estimated to have lived 3.8–3.5 billion years ago (Glansdorff et al., 2008).”

    From The Astrobiology Primer v2.0 (2016) · cites this paper as Glansdorff et al., 2008

    The ‘Palaeochemistry and chronology of early eukaryote evolution’ section discusses a contested estimate of 3.46 billion years ago for the onset of methanogenesis, not a date for LUCA. Searches for 3.8, 3.5, and LUCA’s age found no passage in our copy estimating that LUCA lived 3.8–3.5 billion years ago. Page numbers were not available. (LLM, conf=0.76)

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Research works printed but not linked: 8

  1. Kauffman SA The Origins of Order 1993 Oxford: Oxford University Press
  2. Forterre P Philippe H Where is the root of the universal tree of life? Bioessays 1999 21 871 879 10497338 10.1002/(SICI)1521-1878(199910)21:10<871::AID-BIES10>3.0.CO;2-Q · DOI
  3. Glansdorff N Xu Y Gerday C, Glansdorff N Phylogeny of extremophiles Extremophilies in Encyclopedia of Life Support Systems (EOLSS) 2004 Developed under the Auspicies of the UNESCO, Eolss Publishers, Oxford, UK
  4. Kandler O The early diversification of life Nobel Symposium No 84, Early Life on Earth 1994 Columbia University Press, New York NY 152 160
  5. Forterre P Gerday C, Glansdorff N Strategies of extremophily in nucleic acids adaptation to high temperature Extremophilies in Encyclopedia of Life Support Systems (EOLSS) 2004 Developed under the auspicies of the UNESCO, Eolss Publishers, Oxford, UK
  6. Sakmann E Hoppe W, Lohmann W, Markl H, Ziegler H Physikalische Grundlagen der molekularen Organisation und Dynamik von Membranen Biophysik 1982 2 Springer, Berlin, Germany 439 471
  7. Jensen RA Neidhardt DCFC Evolution of metabolic pathways in enteric bacteria Escherichia coli and Salmonella: Cellular and Molecular Biology Washington: American Society for Microbiology press 2649 2662
  8. Wachtershauser G Before enzymes and templates Microbiol Rev 1988 52 452 484 3070320 PMC373159

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Authors
Glansdorff, N., Xu, Y., & Labedan, B.
Affiliations
  • Vrije Universiteit Brussel (BE)
  • Université Paris-Sud (FR)
Corresponding author
Labedan, Bernard
Venue
Biology Direct
Published
2008-07-09
Volume
3
Issue
1
Pages
29-29
ISSN
1745-6150 (ISSN-L)
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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 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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