Evo Edu Outreach (2012) 5:382–388 DOI 10.1007/s12052-012-0444-8 ORIGIN OF LIFE Cenancestor, the Last Universal Common Ancestor Luis Delaye & Arturo Becerra Published online: 2 September 2012 # Springer Science+Business Media, LLC 2012 Abstract Darwin suggested that all life on Earth could be One Ancestor “tous pour un, un pour tous” phylogenetically related. Modern biology has confirmed Darwin’s extraordinary insight; the existence of a universal Common ancestry is a central idea in biology; its roots can genetic code is just one of many evidences of our common be traced back to the beginning of evolutionary theory. As ancestry. Based on the three domain phylogeny proposed by proof of this, Charles Darwin wrote in the Origin of Species Woese and Fox in the early 1970s that all living beings can Alllivingbeingshavemuchincommon,intheir be classified on one of three main cellular lineages (Ar- chemical composition, their cellular structure, their chaea, Bacteria, and Eukarya), it is possible to reconstruct laws of growth, and their liability to injurious influen- some of the characteristics of the Last Universal Common ces… Therefore, on the principle of natural selection Ancestor or cenancestor. Comparative genomics of organ- with divergence of character, it does not seem incred- isms from the three domains has shown that the cenancestor ible that, from such low and intermediate form both was not a direct descendant of the prebiotic soup nor a animals and plants may have been developed; and, if primitive cellular entity where the genotype and the pheno- we admit this, we must likewise admit that all the type had an imprecise relationship (i.e., a progenote), rather organic beings which have ever lived on this earth it was an organism similar in complexity to extant cells. Due may have descended from someone primordial form. to the process of horizontal gene transfer and secondary gene losses, several questions regarding the nature of the Present-day biology, including biochemistry, molecular cenancestor remain unsolved. However, attempts to infer its phylogeny, and comparative genomics, has confirmed nature have led to the identification of a set of universally Darwin's extraordinary insight, i.e., that all living beings conserved genes. The research on the nature of the last descent ultimately from a single species. universal common ancestor promises to shed light on fun- The modern research on the nature of the last common damental aspects of living beings. ancestor (LCA) or cenancestor (Fitch and Upper 1987)is obviously a major trend in present biology (Morange 2009, Keywords Last universal common ancestor . Cenancestor . 2011) and began with the first attempt to reconstruct a univer- Progenote . Bacteria . Archaea . Eukarya . Horizontal gene sal phylogenetic tree by using a single molecule common to transfer . Early evolution of life all cells. In the mid-1970s, Woese and Fox (1977)compared the small subunits of ribosomal RNA (16/18S rRNA) sequen- L. Delaye ces from different species, including prokaryotes (cells with- Departamento de Ingeniería Genética, out a nuclear membrane) and eukaryotes (cell with a nuclear Centro de Investigación y Estudios Avanzados del Instituto membrane). These comparisons led to the reconstruction of a Politécnico Nacional, trifurcated, unrooted tree in which all known organisms can be Km. 9.6 Libramiento Norte Carretera Irapuato-León, Irapuato, Guanajuato 36821, Mexico grouped in one of three major monophyletic cell lineages; these were named as the domains Eubacteria (now Bacteria), A. Becerra (*) Archaeabacteria (now Archaea), and the nucleo-cytoplasmic Facultad de Ciencias, UNAM, component of Eukaryotes (now known simply as Eucarya; Apdo. Postal 70-407, Ciudad Universitaria, México, D.F. 04510, Mexico Fig. 1). As shown, these lineages are derived from a common e-mail: [email protected] ancestor (Woese et al. 1990). Evo Edu Outreach (2012) 5:382–388 383 Fig. 1 Three cellular domains. Nucleo-cytoplasmic Bacteria The universal tree of life as component of Eukaryotes animals suggested by the 16SrRNA proteobacteria firmicutes molecule fungi plants spirochetes cyanobacteria protists Euryarchaeota Crenarchaeota Archaea Information from one single molecular marker does not that the last common ancestor (LCA) was a progenote was necessarily yield a precise reconstruction of evolutionary pro- disputed when the analysis of homologous traits found cesses, but as indicated by many phylogenies constructed among some of its descendants suggested that it was not a from other genes such as those encoding polymerases, ATPase protocell or any other pre-life progenitor system (Lazcano et subunits, elongation factors, and ribosomal proteins. The al. 1992) but an organism similar in complexity to ext\ant identification of the three major lineages is not an artifact prokaryotes. based exclusively on the reductionist extrapolation of infor- In those years, the inventory of such shared traits was mation derived from a single gene (i.e., the 16SrRNA) but a small, but it was surmised that the sketchy picture developed true reflection of a common ancestry of all living forms. This with the limited data bases would be confirmed when there is in accordance with the fact that all organisms share the were completely sequenced cell genomes from the three same genetic code and crucial features of genome replication, primary domains. This has not been the case: the availability gene expression, membrane-associated ATPase-mediated en- of an increasingly large number of completely sequenced ergy production, and basic anabolic reactions. Minor varia- cellular genomes has sparked new debates, rekindling the tions in the previous process can be easily explained as the discussion on the nature of the ancestral entity (Doolittle outcome of divergent processes from an ancestral life form of 2000). This is shown, for instance, in the diversity of names the three major biological domains (Delaye et al. 2001; that have been coined to describe it: progenote (Woese and Becerra et al. 2007). Fox 1977), cenancestor (Fitch and Upper 1987), last univer- Phylogenetic analysis of rRNA sequences is acknowl- sal cellular ancestor (Philippe and Forterre 1999), and last edged as a prime force in systematics and from its very common community (Line 2002), among others. These inception, had a major impact in our understanding of cel- terms are not truly synonymous, and they reflect the current lular evolution. As exposed by the unrooted rRNA trees, no controversies on the nature of the universal ancestor and the single domain predates the other two, and all three derive evolutionary processes that shaped it. from a common ancestor. Recognition of the differences that exist between the transcriptional and translational machin- eries of the Bacteria, Archaea, and Eucarya, which were Reconstructing the Cenancestor assumed to be the result of independent evolutionary refine- ments, led to the conclusion that the primary branches were As mentioned above, all life on Earth uses exactly the same the descendants of a progenote, a hypothetical biological code to translate the information stored in DNA into pro- entity in which phenotype and genotype still had an impre- teins (with a few exceptions that are clearly evolutionary cise, rudimentary linkage relationship (Woese and Fox novelties). How is it possible that organisms as different as 1977). That is a biological entity where the phenotype and oak trees, Escherichia coli bacterium, amoebas, or ourselves genotype are the same, i.e. a much simpler biological entity share the same set of rules to read (translate) DNA? The than any extant cell. From an evolutionary point of view, it answer is common ancestry; much in the same way that is reasonable to assume that at some point in time the sisters and brothers resemble each other, features shared by ancestors of all forms of life must have been less complex all living beings were inherited from common ancestral than even the simpler extant cells. However, the conclusion species that lived millions of years ago. 384 Evo Edu Outreach (2012) 5:382–388 We can use this knowledge to infer some features of the the cenancestor. The precision of our reconstructions of the biology of this universal ancestor, or cenancestor. But in genome (and therefore our inferences about their biology) of order to do such reconstruction, we need an evolutionary the last universal common ancestor depends on the relative tree describing the phylogenetic relationships among all intensity of previous processes. For instance, the amount of living beings on Earth. As mentioned, such a tree was horizontal gene transfer among prokaryotes is still hotly de- proposed in the early 70's by Woese and Fox when using bated among researchers today (Glansdorff 2000; Gogarten the 16SrRNA molecule to infer the phylogenetic relation- and Townsend 2005; Zhaxybayeva and Doolittle 2011). ships among organisms (Woese and Fox 1977). Before the Despite the methodological difficulties outlined above, work done by Woese and Fox, there were two main classi- different attempts to reconstruct the nature of the last uni- fication systems. In one of them, organisms were classified versal common ancestor have led to the identification of a as Eukaryotes if their genetic material was compartmental- set of highly conserved genes among all cells that very ized by a membrane into a nucleus, or Prokaryotes if this likely have been inherited from the cenancestor (Kyrpides structure is absent (Chatton 1938); in the