Darwin theorized that all extant life forms originated from a unique ancestor, which is now commonly referred to as the LUCA (last universal common ancestor). Koonin's seminal book vindicated Darwin's conjecture on the common origin of life and discussed the reconstruction of the gene repertoire of the LUCA (Koonin, 2011b
). Indeed, comparative genomics revealed the universal conservation of hundreds of genes that are involved in gene expression and are thereby evidence in support of a common ancestral heritage (Koonin, 2003
; Mirkin et al., 2003
). The universally conserved features include the genetic code, i.e., the 64 codons that encode 20 amino acids and the stop signals; the three core subunits of the RNA polymerase; and the translation machinery composed of approximately 30 tRNAs, several translation factors, 18 amino-acyl-tRNA synthetases, and tRNA modification enzymes. Thus, by comparing the genes that present-day organisms have in common, evolutionary genomics indicate that the LUCA was a cellular organism with complete translation machinery, a core transcription system, and several metabolic pathways that included the genes required for purine and pyrimidine nucleotide biosynthesis.
The reconstruction of this ancestral cell is not plausible, because although the ancestor is primitive, its gene repertoire lacks key components that are essential for life (Mirkin et al., 2003
). In particular, it is missing the genes necessary for DNA replication. Moreover, the idea of a common origin for all living beings faces substantial difficulties, including the lack of homology in the core DNA replication system components and the distinct enzymes required for lipid membrane biosynthesis in archaea and bacteria (Leipe et al., 1999
; Pereto et al., 2004
). As for the replication system, it has been hypothesized that the LUCA contained an RNA genome. The replacement of the RNA genome with a DNA genome and the appearance of the corresponding molecule systems would have occurred independently in the three domains of life—archaea, bacteria, and eukarya—after their divergence. Thus, the replication system was thought to have evolved in three distinct DNA viruses (prior to the existence of the DNA cell) and then transferred to the three life domains (Forterre, 1999
). Another scenario is that a LUCA with a DNA genome underwent a subsequent replacement of its DNA-replication systems by non-homologous counterparts in the bacterial, archaeal, and eukaryotic lineages (Forterre, 2002
). Finally, it has been suggested that a non-cellular LUCAS (last universal common ancestral state) existed as a pool of virus-like genetic elements in which the cellular key components originated. Archaea and bacteria might have independently emerged from the LUCAS, likely with numerous life forms now extinct (Koonin, 2009c
). An alternative scenario postulates that the LUCA was a complex, protoeukaryotic lineage with an RNA genome present in a metabolically and morphologically heterogeneous community that gave rise to bacteria and archaea through differential gene loss (Glansdorff et al., 2008
Multiple scenarios have been proposed to explain the origin of living beings. Regardless of which scenario is the most accurate, it has become obvious that the large diversity among species cannot be logically explained only by mutations that occurred on a unique ancestral genome (“descent with modification”). Likewise, the idea of a single mating pair at the origin of all human beings present on earth today cannot be accepted (Raoult, 2011
). Several geneticists agree that “Eve” was not the only woman to conceive children who are ancestors of the current human population. Human evolution appears to be much more chimerical. Add to this, the theory of endosymbiosis showed that mitochondria were of bacterial origin from a species closely related to the Rickettsiales. Darwins reluctantly allowed for the principle of endosymbiosis but limited it to a single event suggesting that the exception does not undermine the principle of a common ancestor. However, we recently demonstrated that mitochondria were not the result of a single event but rather resulted from multiple events of gene transfer from different sources, leading to variation among organisms (Georgiades and Raoult, 2011
). Mitochondria seem to have different bacterial origins, which are mainly, but not exclusively, from the group of Rickettsiales. Similarly, human beings are chimeras that contain retroviral DNA and many genes of bacterial and archaeal origin (Raoult, 2011
). Genes from Trypanosoma cruzi
are likely to integrate into the genome of infected patients and to be passed on to children according to infective heredity. Finally, giant viruses were shown to be chimeras composed of the genes of viral, bacterial, archaeal, and eukaryotic origins (Boyer et al., 2009
). The notion of common ancestry completely undermines the existence of chimeras. Chimerism seems to give a clearer view of genome evolution than does common ancestry.
The hypothesis of a LUCA as a living organism with a ribosome has never been demonstrated. Livings have been classified into three domains commonly known as the Bacteria, the Archae, and Eukaryotes on the basis of ribosomal RNA sequences (Woese et al., 1990
; Pace, 2006
); viruses were excluded from this classification because they do not seem to possess a core of genes related pathogenicity and they lack ribosomes (Moreira and Lopez-Garcia, 2009
). The idea of defining the livings based on the analysis of ribosomal genes implies that all genes are derived from a ribosome-containing organism. However, metagenomic studies that test all of the sequences in an environment show that only 15% of the sequences identified in these conditions can be linked to a cell with a ribosome. These sequences have different origins, some are viral, and others are of unknown origin. These last sequences may be either from viruses that have not yet been identified or genes that were created de novo
(ORFans). In the other hand, the core genome of nucleocytoplasmic large DNA viruses was shown to be as ancient as the other domains of life (Boyer et al., 2010
; Colson et al., 2012
). Thus, asserting that life began with the existence of a ribosome and is defined by this (Moreira and Lopez-Garcia, 2009
) is a form of neo-creationism. Indeed, Woese and Crick (Woese, 1967
; Crick et al., 1976
; Andersson and Kurland, 1990
) proposed that translation started long before the ribosome creation. The initial synthesis of polypeptides did not require the elaborate machinery of ribosomes, activating factors, and enzymes, but was rather accomplished using only RNA messenger and a few primitive tRNAs. This confirms that there was life before the ribosome-containing “LUCA.” Therefore, current cells with ribosomes have incorporated sequences from viruses, newly created genes and sequences predating the ribosome apparition. All these data are contradicting the LUCA theory of a single ancestor of all currently living organisms.
Given what we know about microbiology, a scenario based on the theory of punctuated equilibrium is more likely than the Darwinian phyletic gradualism. According to Gould, long periods of relative evolutionary stability, called “stasis,” are interrupted by evolutionary changes that occur relatively rapidly (Eldredge and Gould, 1972
; Gould, 2002
). Some chaotic changes, such as, geological catastrophes, can be destructive steps that create a bottleneck with few survivors. It is likely that during the evolution of life there was a catastrophic event that created a bottleneck, and the surviving cells had a ribosome and, potentially, a repertoire of ancestral genes other than those encoding the ribosome, particularly the genes encoding for RNA polymerase. The selection process resulting from the bottleneck is completely random and is not influenced by the genes that may confer a greater likelihood of survival in the ecosystem. Survival of a disaster may not confer further evolutionary advantages and can in no way be regarded as natural selection of the fittest. Rather, this process is a non-directional selection without an adaptive goal; is merely chance. Migration from the area of a bottleneck gives rise to increased diversity and the creation of new species. Heterogeneous populations result from the accumulation of mutations and LST. From time to time, a stochastic event may create a new stage and induce the proliferation of a species in an ecosystem. Thus, the capacity of specialized bacteria to multiply is linked to a limited number of events; one event that seems to be particularly important is the limitation of translation capabilities. Indeed, in at least seven bacterial phyla, the evolutionary history of specialized bacteria seems to begin with the disappearance or the malfunction of the ribosomal operon, which forced the bacterium to specialize while limiting its production only to useful proteins. This change allows the specialized bacteria to expand more rapidly than others in their specific niche (Merhej et al., 2009
). However, the gene repertoires of living beings did not completely disappear but some have been used and are present in a certain number of organisms that exist today. Thus, genes have an evolutionary history that is different from that of the whole organism, as postulated by Dawkins (2006
Our hypothesis is that ancestral organisms were sorted by successive disasters, and some of them were able to improve their ability to live in the ecosystems in which they now live. These species represent chimeras made by combining ancestral genes with laterally acquired sequences, a mixture of genes that have been recycled from organisms that are now extinct, and genes that were newly created (Figure ). The idea of a unique common ancestor denies chimerism and traces the creative origin of life today to an event. Many scientists adhere to this theory and end up denying the very existence of life outside of cells with a ribosome such as, viruses that may be excluded from “life.” In contrast, we believe that life cannot be considered anything other than the expression of the language contained in genetic sequences.
Proportion of the ORFans and potential lateral transfer in bacterial genomes.