Did DNA replication evolve twice independently?

“Nonorthologous displacement affects all functional classes of genes, with striking examples seen even among the most fundamental functions, such as DNA replication, where the principal replicative enzymes are nonhomologous in archaea and bacteria (64,65).”

“Even the chemical nature of cell walls that make prokaryotic plasma membranes turgor resistant (Kandler & König 1998) and the mechanisms of DNA maintenance differ among eubacteria and archaebacteria (Leipe et al. 1999; Poole & Logan 2005).”

“Forterre's proposal is based on the well-known observation that the DNA replication systems of archaea and bacteria are, largely, unrelated, making it unlikely that LUCA had a DNA genome [58-60].”

“More specifically, the absence of an ancestral DNA polymerase and associated replication enzymes in the LUCA suggest that it probably had a system of replication involving reverse transcription [127].”

“Although a detailed examination of the reconstructed gene-sets is not possible here, it is interesting to note that the reconstructed gene-set of LUCA (within a broad range of g values) lacks some of the main components of the DNA-replication machinery (such as the replicative polymerase and helicase), in agreement wi…”

“Surprisingly, the central components of these systems (DNA polymerases, primases and replicative helicases) are either unrelated or, at least, not orthologous in archaebacteria and eubacteria [44, [49] [50] [51] [52] .”

“This is likely to reflect radical innovation at these evolutionary junctures, perhaps including even independent origin of DNA replication systems [61,71,72].”

“This archaeo-bacterial dichotomy is similar to that in some families of proteins involved in DNA replication, such as PCNA/DNA polymerase III b subunit and ATP/NAD-dependent DNA ligase (75,76).”

“Such differences include: (i) their membrane lipids (isoprene ethers versus fatty acid esters) [123], (ii) their cell walls (peptidoglycan versus S-layer) [124], (iii) their DNA maintenance machineries [116,125], (iv) the 31 ribosomal proteins that are present in archaebacteria but missing in eubacteria [126,127] (v)…”

“This situation also seems to be true for the DNA replication machinery, which is very different in archaea and bacteria but shares some common elements [ 36 ,37].”

“As examples of the latter, DNA primase, DNA polymerization activity, and ribonuclease H activity all appear to have multiple independent origins (Leipe et al. 1999).”

“A wide range of theories have been put forward to account for this observation, ranging from the proposal that DNA replication arose twice in cellular organisms, suggesting that the last common ancestor of all living organisms may not have had a DNA genome, to the possibility that the last common ancestor had a define…”

“However, the phyletic patterns of the cellular members of the AEP superfamily do not seem to indicate that this enzyme was present in LUCA.”

“Under this model, the primordial genetic pool is believed to have evolved from a pure RNA world to a RNA-protein system to the modern world of the Central Dogma (DNARNA-protein) through an intermediate stage, possibly, corresponding to the LUCA, at which a retrovirus-like cycle of replication became widespread[96,97].”

“Hence, considerable diversity of protein domains appears to have emerged prior to the "crystallization" [95] of a transcription machinery similar to the one that operates in modern cells and probably had been already in place in LUCA [96].”

“If LUCA had a RNA genome and DNA synthesis was invented twice [11,60], we could consider the possibility that a membraneous compartment (let us call it a protonucleus) had already formed autogenously around the primeval RNA genome, so that the nucleus itself would not necessarily have emerged twice independently.”

“In particular, the core components of the DNA replication machinery are non-homologous (or, at least, non-orthologous) in bacteria, on the one hand, and archaea and eukaryotes, on the other hand (176).”

“There are presently two cellular versions of the symmetric DNA replication mechanism, one in Bacteria, another one in Archaea/Eukarya [26,31,32].”

“Despite the clear functional conservation of core replisomal activities, the helicases and primase/polymerases used for replicating DNA have evolved twice independently, with bacteria using one class of enzymes and archaea/eukaryotes using another (2).”

“Thus, plausible, even if conflicting, accounts of the emergence of these systems have been derived from comparative-genomic data and evolutionary reasoning [70,140-144].”

“Distinct helicase mechanisms may require distinct helicase loading mechanisms in bacteria and eukaryotes Surprisingly, whilst DnaA and ORC (subunits 1–5) belong to the same clade of AAA+ ATPases [8], the respective replicative helicases DnaB and Mcm2-7 are not orthologous [9].”

“Most likely, retroelements have been an integral part of biological systems since the stage of the primordial replicators, when they actually gave rise to the first DNA genomes (125).”

“In both the Bacteria and Archaea, non-homologous enzyme complexes for DNA replication (Leippe et al. 1999) with coordinated leading strand and lagging strand synthesis departed from the much simpler system of rolling circle replication of the pre-cells, perhaps under the directing influence of the two different kinds…”

“…a nucleotidyltransferase involved in copying its genomic nucleic acid; it has been proposed that such copying proceeded via an RNA intermediate (Leipe et al. 1999), and that said nucleotidyltransferase more than likely was of the palm-domain ferredoxin-like fold, consisting of four- or…”

“For example, most enzymes involved in DNA replication are not homologous in bacteria and archaea (Edgell and Doolittle 1997; Leipe et al. 1999).”

“…when compared with archaea and eukarya, in marked contrast to the considerable orthology found for proteins of the other two major information processing systems – translation and transcription – in all three domains (Edgell & Doolittle, 1997; Leipe et al., 1999; Tye, 2000; Woese, 2000, 2002).”

“Although a crystal structure of residues 1–197 demonstrates that α subunit folds into the right-hand shape characteristic of DNA polymerases [282], the absence of significant sequence similarities between Pol III α and well-known DNA polymerases leaves DNA binding domains unclear [283].”

“Archaea contain a PCNA clamp and an RFC clamp loader that function with B-family DNA polymerase”

“…eukaryotic kingdoms, there has been significant evolutionary diversification of the molecules that complete each task, to the point where it is now clear that aspects of the replicative machinery emerged twice, independently, during cellular evolution (Edgell & Doolittle, 1997; Leipe et al., 1999).”

“Martin and colleagues recently reported a lack of correspondence between individual protein trees and the concatenation tree in several datasets of archaeal and bacterial proteins (Thiergart et al., 2014).”

“…in the form of homologous inserts in conserved proteins, indicate that, for the majority of these genes, the preferred tree topology is one with the eukaryotic branch placed outside the extant diversity of archaea although small subsets of genes show crenarchaeal and euryarchaeal affinities.”

“Within the unitary populations of the Bacteria and Archaea enzyme complexes for modern DNA replication ( Leippe et al ., 1999 ) with co-ordinated leading strand and lagging strand synthesis departed independently from the much simpler system of rolling circle replication of the pre-cells.”

“some of their central components probably evolving independently in the two principal lines of descent.(9)”

“ion pumping [13], and even DNA replication [14].”

“This is perhaps surprising in view of the fact that Archaea have important similarities to Eukarya, notably enzymes involved in DNA replication (47).”

“It is especially unclear whether RNA entities ever evolved genomes close to the 100–300 kilobase (kb) range [2, 3] of the “minimal” reconstructed cellular DNA genome [4].”

“They are essential to viral replication and present a unique evolutionary fate of being the only replicative RdRps preserved from the RNA world (Leipe et al., 1999).”

“This scenario is in agreement with the idea of a LUCA with an RNA genome((50))”

“(i) did not have a typical, large DNA genome, 22, 44 and/or (ii) was not a typical membrane-bounded cell (Fig.”

“…thus, the key proteins involved in DNA replication in Archaea and eukaryotes are not homologous to the functionally analogous proteins of Bacteria (Leipe et al. 1999), and conversely, some of the principal enzymes of membrane biogenesis are homologous in eukaryotes and Bacteria but not in…”

“Subsequently, the notion of a "communal ancestor" has been developed into a specific scenario [16,19] that derived from the comparative-genomic indications that the enzymes of membrane biogenesis and the core DNA replication machineries in archaea and bacteria were nonhomologous [18,42].”

“The fact that the replicative DNA polymerases (DNAPs) of bacteria, archaea and eukaryotes are not homologous has prompted ideas of an RNA-based LUCA 31,34,35 .”

“This is especially striking in the case of DNA replication, since archaeal genomes encode homologues of nearly all eukaryal DNA replication proteins but only one homologue of a bacterial DNA replication protein (Edgell and Doolittle, 1997; Forterre, 1999; Leipe et al., 1999).”

“The replicative polymerases are sharply divided between the bacterial and archaealeukaryotic types that appear not to be homologous [7,8].”

“Together these observations have suggested that molecular processes for DNA replication in Bacteria and Eukarya might have independent origins (Leipe et al., 1999; Forterre, 1999).”

“One of the outstanding questions in Biology is the origin of the two evolutionarily distinct DNA replication systems in bacteria and archaea/eukaryotes, respectively (4,68).”

“This observation led to a hypothesis that the two replicative systems evolved twice independently from a common ancestor which utilized reverse transcription to replicate an RNA/DNA genome (27) (Figure 3A).”

“Bacterial and bacteriophage primases of the DnaG family have no apparent relationship to eukaryotic and archaebacterial primases, or to any other RNA or DNA polymerases (Aravind et al., 1998; Leipe et al., 1999).”

“However, many genes encoding proteins sharing sequence similarities with eukaryotic DNA replication proteins are present in all archaeal genomes (Olsen and Woese, 1997; Edgell and Doolittle, 1997; Ishino and Cann, 1998; Cann and Ishino, 1999, Leipe et al., 1999).”

“This observation led to the hypothesis that replication of doublestranded DNA as the principal form of replication of the genetic material was ‘invented’ twice, independently: once in bacteria and once in the ancestor of archaea and eukaryotes [22,23].”

“taken from the literature (7,69) or are named after the secondary structure elements of PolDelta (Supplementary Figure S1).”

“In particular, the presence of common structural domains in this kind of OBPs, beyond their marginal sequence similarities, leaves the way open to discuss their possible phylogenetic relationships [8,9].”

“Both sequence and structural evidence favors the deepest split among nucleic acid ligases as being between the ATPdependent and NAD-dependent DNA ligases (Figure 6D), which act as the primary DNA ligase respectively in the archaeo-eukaryotic and bacterial clades (292).”

“Generally, the archaeal replication protein core appears to be the same as the eukaryotic core, but eukaryotes typically possess multiple paralogous subunits within complexes that are homomeric in archaea, many additional components interacting with the core ones and more complex regulation (Leipe et al. 1999; Bell an…”

“…and his collaborators analyzed a large set of primases, replicative polymerases, and other proteins involved in DNA replication, and suggested an alternative scheme with a hybrid RNA/DNA cenancestral genetic system whose complex replication cycle involved reverse transcription (Leipe et al., 1999).”

“It has also been hypothesized that LU-CAs may have an RNA genome, or an RNA / DNA hybrid genome, or a DNA genome with an RNA replication intermediate (53,56,57) (Figure 7B).”

“Most structural elements contributing to NTP and DNA binding by the large subunit are located in the C-terminal half of the protein (p58C in human primase) (11, 17–20).”