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Review
, 3, 29

The Last Universal Common Ancestor: Emergence, Constitution and Genetic Legacy of an Elusive Forerunner

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Review

The Last Universal Common Ancestor: Emergence, Constitution and Genetic Legacy of an Elusive Forerunner

Nicolas Glansdorff et al. Biol 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.

Figures

Figure 1
Figure 1
Committing steps in the biosynthesis of membrane lipids. The "primary divide" separating Archaea from Bacteria and Eukarya is outlined.
Figure 2
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.

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