The replicative DNAPs of bacteria, archaea, and eukaryotes belong to 3 distinct protein families, and the core catalytic domains of these 3 DNAPs are unrelated to each other, i. The great majority of dsDNA viruses that infect either prokaryotes or eukaryotes and encode their own rDNAPs have the B family polymerase PolB that is also responsible for the replication in eukaryotes [ 9 ] Table 1.
Archaea encode multiple PolB copies, and with the exception of members of the order Crenarchaeota and some thermophilic members of the Thaumarchaeota [ 10 , 11 ], also the distinct family D DNAP PolD [ 12 , 13 , 14 ]. The structure of PolD has been recently solved, resulting in a surprising discovery that the catalytic core of PolD is homologous to that of the large subunits of the DNA-directed RNA polymerases RNAPs that are responsible for transcription in all three domains of life and many large DNA viruses [ 19 , 20 , 21 ].
These findings seem to shed unexpected light on the evolution of the replication machineries in the three domains of life as well as viruses. They might even help to infer the nature of the replication machinery in the LUCA suggesting an evolutionary scenario in which PolD takes the central stage as the ancestral replicative polymerase.
In the rest of this article, we discuss the reasoning behind this scenario and its implications. Dashed lines indicate regions where insertions into the core palm domains have occurred; these have been omitted for visualization purposes. The homologous relationships among the DNA and RNA polymerases allow us to infer the evolution of the replication and transcription machineries in the 3 domains of life and in viruses. The key relationships are described below and summarized in Table 1 and Fig.
Numerous large viruses with dsDNA genomes, including some tailed bacteriophages as well as nucleocytoplasmic large DNA viruses NCLDV , such as the thoroughly characterized vaccinia virus and the giant mimiviruses, and baculo-like viruses of eukaryotes, also encode RNAPs with two DPBB domain-containing subunits [ 28 , 29 , 30 , 31 , 32 ].
The two large RNAP subunits are also fused in linear cytoplasmic plasmids from plants and fungi [ 37 ], suggesting that such fusions occur repeatedly in the course of RNAP evolution. PolBs are also represented in all archaea [ 12 , 38 ] but appear to function as the main replicative polymerases only in Crenarchaeota [ 39 ]. Additionally, PolBs are encoded by numerous viruses and some non-viral mobile genetic elements from all 3 domains of life [ 9 , 29 , 41 , 42 , 43 ].
Some bacteria encode PolBs of apparent virus origin that are involved in repair functions [ 44 ]. Only a few, poorly characterized phages encode PolC homologs, presumably a late acquisition in virus evolution [ 9 ]. PolA, a distant homolog of PolB, is a bacterial repair polymerase. Some phages, Sputnik-like virophages a group of eukaryotic viruses within the family Lavidaviridae , as well as mitochondria and chloroplasts employ PolA homologs as rDNAPs [ 55 , 56 , 57 , 58 ].
In addition, some phages e. An additional important assumption is the RNA world hypothesis [ 62 , 63 ]. Specifically, we assume a stage in the evolution of life, subsequent to the RNA-only era, when the replicating genomes of the protocellular life forms consisted of RNA including mRNA translated into proteins including RdRPs [ 64 , 65 ].
We assume that translation evolved within the RNA world, giving rise to an RNA-protein world that presaged the advent of DNA as the dedicated information carrier and the DNA replication machinery, probably, via a reverse transcription stage. The evolutionary connections among the polymerases of cellular organisms and viruses can be superimposed over the evolutionary tree of life that is based on the phylogenies of the universal proteins, namely, translation system components and the large RNAP subunits.
Proposed scenario for the origin and early evolution of DNA replication and transcription. The multiple forms of PolB that are present in both archaea and eukaryotes are not shown for the sake of simplicity. Different domains and subunits are indicated with various shapes and colors. Yellow star indicates an active exonuclease domain. Given that all extant polymerases in this lineage contain two DPBB domains, it appears most likely that the primordial replicative polymerase already possessed this characteristic pair of DPBB domains that both contribute essential amino acid residues to the catalytic site.
These domains conceivably evolved via duplication of a single ancestral DPBB domain single DPBB domains are present in a variety of metabolic enzymes [ 21 ] and could have resided in either a single or in two subunits Fig. The ancestral DPBB form that gave rise to the first protein RdRP might have started as a non-catalytic RNA-binding domain that functioned as a cofactor to ribozyme RdRPs, but following the duplication, evolved the polymerase activity and displaced the ribozyme. The separation of the replication and transcription machineries could have been precipitated by the accretion of additional domains in both classes of enzymes.
Additionally, either already in LUCA or at an early stage of archaeal evolution, PolD acquired a distinct small subunit, a phosphoesterase that became the proofreading exonuclease [ 20 , 71 ].
Assuming that the ancestral RdRP contained the two DPBB domains within a single polypeptide, in the transcription lineage, the ancestral two-DPBB enzyme split into the two subunits each of which captured multiple additional domains including a clamp unrelated to PCNA [ 21 , 26 ].
Specifically, PolB could originate from the RT of primordial retroelements. PolBs were similarly acquired by several groups of bacteria, apparently, at later stages of evolution Fig. In most archaea, PolBs are not involved in replication but rather in repair-related functions.
A similar displacement occurred at the onset of the evolution of eukaryotes. The evolution of PolB in eukaryotes also involved inactivation of the small exonuclease subunit archaeal DP1 that retained a structural role. Conceivably, the exonuclease activity of the small subunit became dispensable in eukaryotes due to its functional redundancy with the exonuclease domain of the PolB which replaced the PolD large subunit archaeal DP2 [ 71 ].
The origin of PolA that is conserved in nearly all bacteria and clearly is ancestral in the bacterial domain remains uncertain. One possibility is that PolA was derived from an ancestral RRM polymerase, perhaps, in a virus, and then was captured by the bacterial ancestor. In bacteria, PolA is a repair enzyme that is not directly involved in replication, but it functions as the replicative polymerase in some viruses and in eukaryotic mitochondria.
Notably, PolA was captured by a group of phages as a single-subunit RNAP and was subsequently recruited in the same capacity by eukaryotic mitochondria, in all likelihood, from a phage [ 73 , 74 ].
Thus, recruitment of viral polymerases, which are often more catalytically efficient than cellular counterparts [ 75 , 76 ], by cellular organisms appears to be a recurrent theme in evolution, with postulated replacement of PolD by PolB at the onset of eukaryotes being but one example albeit one of major importance. The origin of DNA replication is one of the most enigmatic subjects in the reconstruction of the early stages in the evolution of life because the replicative DNAPs as well as primases and the main helicases involved in replication are not homologous among bacteria, archaea, and eukaryotes.
Until recently, this lack of conservation of the key elements of the DNA replication machinery precluded reconstruction of the ancestral state, suggesting multiple origins for DNA replication and even the possibility that LUCA was an RNA-based cell [ 2 , 5 ]. However, given the universal conservation of other components of the replication apparatus, such as PCNA sliding clamp , clamp loader ATPase, and ssDNA-binding protein, along with the inferred relatively high complexity of LUCA, comparable to that of modern prokaryotes, such scenarios appear unlikely.
The line of reasoning developed here, based primarily on the recently discovered evolutionary connection between PolD and the universally conserved RNAP, allows inference of the ancestral DNAP. The proposed evolutionary scenario appears parsimonious in that the two key processes associated with the advent of DNA genomes, replication and transcription, derive from a common ancestor.
However, a PolB-centered scenario for the evolution of replication lacks the symmetry in the evolution of replication and transcription. Besides, PolB is the replicative DNAP only in Crenarchaeota, eukaryotes, and in diverse viruses infecting hosts in all three cellular domains which seem to be best compatible with an origin in viruses or mobile genetic elements. Among these evolutionary lineages, the DPBB one is associated with the evolution of cells and the RRM one, with the evolution of viruses and mobile genetic elements.
The causes of such asymmetry between hosts and parasites remain enigmatic. A notable aspect of the emerging picture of the evolution of replication and transcription is the switch between RNA and DNA template and products that, clearly, occurred on multiple occasions in evolution. Although highly challenging, validation of the current evolutionary scenario by experimental reconstruction of ancestral forms of RNA and DNA polymerases does not seem to be out of the question.
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Both processes can lead to errors if an incorrect nucleotide is incorporated. An error in either DNA replication or transcription can cause a change in the gene, by either changing the DNA sequence in one of the daughter cells leading to transcription of the incorrect mRNA sequence, or by causing the mRNA to incorporate an incorrect base pair resulting in the wrong protein sequence being translated. DNA replication occurs in preparation for cell division, while transcription happens in preparation for protein translation.
DNA replication is important for properly regulating the growth and division of cells. The DNA will not replicate if the cell lacks certain growth factors, thereby keeping the cell division rate under control. Transcription of DNA is the method for regulating gene expression. Annunziato, A. Split decision: What happens to nucleosomes during DNA replication? Journal of Biological Chemistry , — Bessman, M. Enzymatic synthesis of deoxyribonucleic acid. General properties of the reaction. Kornberg, A.
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