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

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      1 , 1 , 2 ,
      Biology Direct
      BioMed Central

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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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          Most cited references225

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          Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.

          Molecular structures and sequences are generally more revealing of evolutionary relationships than are classical phenotypes (particularly so among microorganisms). Consequently, the basis for the definition of taxa has progressively shifted from the organismal to the cellular to the molecular level. Molecular comparisons show that life on this planet divides into three primary groupings, commonly known as the eubacteria, the archaebacteria, and the eukaryotes. The three are very dissimilar, the differences that separate them being of a more profound nature than the differences that separate typical kingdoms, such as animals and plants. Unfortunately, neither of the conventionally accepted views of the natural relationships among living systems--i.e., the five-kingdom taxonomy or the eukaryote-prokaryote dichotomy--reflects this primary tripartite division of the living world. To remedy this situation we propose that a formal system of organisms be established in which above the level of kingdom there exists a new taxon called a "domain." Life on this planet would then be seen as comprising three domains, the Bacteria, the Archaea, and the Eucarya, each containing two or more kingdoms. (The Eucarya, for example, contain Animalia, Plantae, Fungi, and a number of others yet to be defined). Although taxonomic structure within the Bacteria and Eucarya is not treated herein, Archaea is formally subdivided into the two kingdoms Euryarchaeota (encompassing the methanogens and their phenotypically diverse relatives) and Crenarchaeota (comprising the relatively tight clustering of extremely thermophilic archaebacteria, whose general phenotype appears to resemble most the ancestral phenotype of the Archaea.
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            A serpentinite-hosted ecosystem: the Lost City hydrothermal field.

            The serpentinite-hosted Lost City hydrothermal field is a remarkable submarine ecosystem in which geological, chemical, and biological processes are intimately interlinked. Reactions between seawater and upper mantle peridotite produce methane- and hydrogen-rich fluids, with temperatures ranging from <40 degrees to 90 degrees C at pH 9 to 11, and carbonate chimneys 30 to 60 meters tall. A low diversity of microorganisms related to methane-cycling Archaea thrive in the warm porous interiors of the edifices. Macrofaunal communities show a degree of species diversity at least as high as that of black smoker vent sites along the Mid-Atlantic Ridge, but they lack the high biomasses of chemosynthetic organisms that are typical of volcanically driven systems.
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              Phylogenetic classification and the universal tree.

              From comparative analyses of the nucleotide sequences of genes encoding ribosomal RNAs and several proteins, molecular phylogeneticists have constructed a "universal tree of life," taking it as the basis for a "natural" hierarchical classification of all living things. Although confidence in some of the tree's early branches has recently been shaken, new approaches could still resolve many methodological uncertainties. More challenging is evidence that most archaeal and bacterial genomes (and the inferred ancestral eukaryotic nuclear genome) contain genes from multiple sources. If "chimerism" or "lateral gene transfer" cannot be dismissed as trivial in extent or limited to special categories of genes, then no hierarchical universal classification can be taken as natural. Molecular phylogeneticists will have failed to find the "true tree," not because their methods are inadequate or because they have chosen the wrong genes, but because the history of life cannot properly be represented as a tree. However, taxonomies based on molecular sequences will remain indispensable, and understanding of the evolutionary process will ultimately be enriched, not impoverished.
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                Author and article information

                Journal
                Biol Direct
                Biology Direct
                BioMed Central
                1745-6150
                2008
                9 July 2008
                : 3
                : 29
                Affiliations
                [1 ]JM Wiame Research Institute for Microbiology and Vrije Universiteit Brussel, 1 ave E. Gryzon, B-1070 Brussels, Belgium
                [2 ]Institut de Génétique et Microbiologie, Université Paris Sud, CNRS UMR 8621, Bâtiment 400, 91405 Orsay Cedex, France
                Article
                1745-6150-3-29
                10.1186/1745-6150-3-29
                2478661
                18613974
                d1ec2b3d-a716-4659-9da3-5f05b4ca994a
                Copyright © 2008 Glansdorff et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 24 June 2008
                : 9 July 2008
                Categories
                Research

                Life sciences
                Life sciences

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