The DOI matches its Crossref record; 66 of the 66 references it cites were found in a registry or an index.
Did DNA replication evolve twice independently?
Open accessAbstract
DNA replication is central to all extant cellular organisms. There are substantial functional similarities between the bacterial and the archaeal/eukaryotic replication machineries, including but not limited to defined origins, replication bidirectionality, RNA primers and leading and lagging strand synthesis. However, several core components of the bacterial replication machinery are unrelated or only distantly related to the functionally equivalent components of the archaeal/eukaryotic replication apparatus. This is in sharp contrast to the principal proteins involved in transcription and translation, which are highly conserved in all divisions of life. We performed detailed sequence comparisons of the proteins that fulfill indispensable functions in DNA replication and classified them into four main categories with respect to the conservation in bacteria and archaea/eukaryotes: (i) non-homologous, such as replicative polymerases and primases; (ii) containing homologous domains but apparently non-orthologous and conceivably independently recruited to function in replication, such as the principal replicative helicases or proofreading exonucleases; (iii) apparently orthologous but poorly conserved, such as the sliding clamp proteins or DNA ligases; (iv) orthologous and highly conserved, such as clamp-loader ATPases or 5'-->3' exonucleases (FLAP nucleases). The universal conservation of some components of the DNA replication machinery and enzymes for DNA precursor biosynthesis but not the principal DNA polymerases suggests that the last common ancestor (LCA) of all modern cellular life forms possessed DNA but did not replicate it the way extant cells do. We propose that the LCA had a genetic system that contained both RNA and DNA, with the latter being produced by reverse transcription. Consequently, the modern-type system for double-stranded DNA replication likely evolved independently in the bacterial and archaeal/eukaryotic lineages.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Specifically, the last common ancestor may have had a cell membrane (Jékely 2006;Koga 2011;Lombard et al. 2012;Sojo et al. 2014;Coleman et al. 2019), RNA and phosphodiester-based energy coupling (e.g.Werner and Grohmann 2011), as well as thioester-based intermediary metabolism (Goldford et al. 2017;Weiss et al. 2018), but may not have used a strictly DNA genome (Mushegian and Koonin 1996;Leipe et”
From The Emergence of Life (2019) · cites this paper as Leipe et al. 1999
In the citing paper
“The fact that the mechanisms of DNA replication in bacteria and archaea are different [133] suggests the possibility that DNA, as the primary information storage molecule, evolved independently in each of these lineages [133,134,135].”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [134]
Citations
Cites
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302
A genomic perspective on protein families.
Tatusov, R., Koonin, E., & Lipman, D. (1997) · Science · doi:10.1126/science.278.5338.631 · Cited by 3,777
Self-citationCrystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor
Kohlstaedt, L. A., Wang, J., Friedman, J. M., Rice, P. A., & Steitz, T. A. (1992) · Science · doi:10.1126/science.1377403 · Cited by 1,914
Neuwald, A. F., Aravind, L., Spouge, J. L., & Koonin, E. V. (1999) · Genome Research · doi:10.1101/gr.9.1.27 · Cited by 1,840
Self-citationHelicases: amino acid sequence comparisons and structure-function relationships
Gorbalenya, A. E., & Koonin, E. V. (1993) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(05)80116-2 · Cited by 1,160
Self-citationWoese, C. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.6854 · Cited by 1,053
Conservation of gene order: a fingerprint of proteins that physically interact
Dandekar, T. (1998) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(98)01274-2 · Cited by 1,047
An atypical topoisomerase II from archaea with implications for meiotic recombination
Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.-C., Nicolas, A. G., & Forterre, P. (1997) · Nature · doi:10.1038/386414a0 · Cited by 948
Murzin, A. G. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05726.x · Cited by 929
A minimal gene set for cellular life derived by comparison of complete bacterial genomes
Mushegian, A. R., & Koonin, E. V. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.19.10268 · Cited by 916
Self-citation
Research works printed but not linked: 2
- 1997, ISMB, 5, 333
- 1997, Biokhimii a (Moscow, Russia), 62, 1202
Cited by
Sorted by citations
Items 101–200 of 351
Intein Clustering Suggests Functional Importance in Different Domains of Life
Novikova, O., Jayachandran, P., LeSassier, D. S., Morton, Z., Merwin, S., Topilina, N. I., & Belfort, M. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv271 · Cited by 82
“In contrast, the core components of transcription and translation are highly conserved in all domains of life (Edgell and Doolittle 1997; Leipe et al. 1999), and they contain few inteins.”
BackgroundInfluentialBocquier, A. A., Liu, L., Cann, I., et al. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00119-1 · Cited by 80
Chromosome replication, nucleoid segregation and cell division in Archaea
Bernander, R., & Bernander, R. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01760-1 · Cited by 79
Caspi, R., Pacek, M., Consiglieri, G., et al. (2001) · The EMBO Journal · doi:10.1093/emboj/20.12.3262 · Cited by 78
Hecker, A., Leulliot, N., Gadelle, D., Graille, M., Justome, A., Dorlet, P., Brochier‐Armanet, C., Quevillon‐Chéruel, S., Cam, É. L., TILBEURGH, H. V., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm554 · Cited by 75
“Several authors suggested that the last universal ancestor of the three domains of life, LUCA, had an RNA or RNA/DNA genome, and that most proteins involved in DNA metabolism only appeared after the divergence of the major cellular lineages (34,35).”
BackgroundČuboňová, L., Richardson, T. T., Burkhart, B. W., Kelman, Z., Connolly, B. A., Reeve, J. N., & Santangelo, T. J. (2013) · Journal of Bacteriology · doi:10.1128/jb.02037-12 · Cited by 76
Alley, S. C., Ishmael, F. T., Jones, A. D., & Benkovic, S. J. (2000) · Journal of the American Chemical Society · doi:10.1021/ja000591t · Cited by 72
Takeuchi, N., Hogeweg, P., & Koonin, E. V. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002024 · Cited by 69
“, the universality of the translation machinery in all domains of life suggests that proteins most likely evolved in the RNA world before DNA (e.g.,”
BackgroundSelf-citationCdc45: the missing RecJ ortholog in eukaryotes?
Sánchez‐Pulido, L., & Ponting, C. P. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr332 · Cited by 71
Biochemical Analysis of Replication Factor C from the Hyperthermophilic ArchaeonPyrococcus furiosus
Cann, I., Ishino, S., Yuasa, M., et al. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.8.2614-2623.2001 · Cited by 69
“Several genes encoding eukaryotic-like DNA replication proteins are present in archaeal genomes (4, 7, 12, 24).”
BackgroundMatsumiya, S., Ishino, S., Ishino, Y., et al. (2002) · Genes to Cells · doi:10.1046/j.1365-2443.2002.00572.x · Cited by 68
“Recent sequence analyses of the complete genomes from several organisms in Archaea, the third domain of life, confirmed that the proteins relating to the genetic information system, including DNA replication, are structurally more similar to eukaryotic proteins than those from Bacteria (reviewed in Edgell & Doolittle…”
BackgroundEvolution of replication machines
Yao, N. Y., & O’Donnell, M. E. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1125845 · Cited by 68
“Viruses may have predated cells (Forterre et al., 2004; Koonin et al., 2015; Leipe et al., 1999), and thereby provided a large pool of genetic diversity that homologous recombination could plumb for genes and ultimately splice them together into a genome that encodes sufficient chemistry to enable…”
BackgroundMethodInfluentialOberto, J., Breuil, N., Hecker, A., et al. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp557 · Cited by 66
“proteins are known to be involved in DNA metabolism (46).”
BackgroundA Natural Classification of Ribonucleases
Aravind, L., & Koonin, E. V. (2001) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(01)41142-6 · Cited by 65
Self-citationThe Last Universal Common Ancestor (LUCA) and the Ancestors of Archaea and Bacteria were Progenotes
Giulio, M. D. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9407-2 · Cited by 63
“observations that DNA originated late on, only after the main phyletic lines of divergence were established (Mushegian and Koonin 1996; Aravind et al. 1999; Freeland et al. 1999; Leipe et al. 1999; Poole and Logan 2005; Forterre 2005, 2006; Di Giulio 2006a; Glansdorff et al. 2008).”
BackgroundSystems biology perspectives on minimal and simpler cells
Xavier, J. C., Patil, K. R., & Rocha, I. (2014) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00050-13 · Cited by 58
“In a comparison of sequences of proteins involved in DNA replication, it was proposed that the LUCA had a genetic system that contained both RNA and DNA, but the latter was, at that time, produced by reverse transcription (83).”
BackgroundStructural Mechanisms for Replicating DNA in Eukaryotes
Attali, I., Botchan, M. R., & Berger, J. M. (2021) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-090120-125407 · Cited by 65
Optical tweezers experiments resolve distinct modes of DNA‐protein binding
McCauley, M. J., & Williams, M. C. (2008) · Biopolymers · doi:10.1002/bip.21123 · Cited by 60
Gene content of LUCA, the last universal common ancestor
Mushegian, A. (2008) · Frontiers in Bioscience · doi:10.2741/3031 · Cited by 61
Koonin, E. V. (2006) · Biology Direct · doi:10.1186/1745-6150-1-39 · Cited by 59
“We can thus suppose, from the principle of actualism, that many cellular lineages also disappeared both during the evolution from the first cells to LUCA or from LUCA to the modern cellular world.”
BackgroundInfluentialSelf-citationBideshi, D. K., Demattei, M.-V., Rouleux‐Bonnin, F., Stasiak, K., Tan, Y., Bigot, S., Bigot, Y., & Federici, B. A. (2006) · Journal of Virology · doi:10.1128/jvi.01639-06 · Cited by 58
“SfAV encodes a DNA polymerase (ORF 1) of the B family, which, like the principal replication enzymes in prokaryotes and eukaryotes, contains a nucleotide-polymerizing domain (II-VI-III-I-V) fused to an N-terminal 3 to 5 exonuclease domain (67).”
BackgroundPisani, F. M., Felice, M. D., Carpentieri, F., et al. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3964 · Cited by 58
Brochu, J., Vlachos-Breton, É., Sutherland, S., et al. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007668 · Cited by 55
Grúz, P., Pisani, F. M., Shimizu, M., Yamada, M., Hayashi, I., Morikawa, K., & Nohmi, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107213200 · Cited by 55
Screening strategies for discovery of antibacterial natural products
Singh, S. B., Young, K., & Miesel, L. (2011) · Expert Review of Anti-infective Therapy · doi:10.1586/eri.11.81 · Cited by 56
Molecular evolution before the origin of species
Davis, B. K. (2002) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(02)00012-3 · Cited by 55
“…RNA polymerase and 50-30 flap exonuclease (FEN-1), exhibit significant sequence homology among bacteria, archaea and eukaryote sources, as required of pre-divergence proteins (Gropp et al., 1986; Sweetser et al., 1987; Langer et al., 1995; Edgell and Doolittle, 1997; Leipe et al., 1999; Section 4).”
BackgroundInfluentialUncovering major genomic features of essential genes in Bacteria and a methanogenic Archaea
Grazziotin, A. L., Vidal, N. M., & Venancio, T. M. (2015) · The FEBS Journal · doi:10.1111/febs.13350 · Cited by 42
The origin of modern terrestrial life
Forterre, P., & Gribaldo, S. (2007) · HFSP journal · doi:10.2976/1.2759103 · Cited by 73
“To explain this observation, Koonin and colleagues have suggested that LUCA had an RNA genome, but used DNA as a replication intermediate (much like a retrovirus) (Leipe et al., 1999).”
BackgroundType IA topoisomerases can be “magicians” for both DNA and RNA in all domains of life
Ahmad, M., Xu, D., & Wang, W. (2017) · RNA Biology · doi:10.1080/15476286.2017.1330741 · Cited by 51
“sist of organisms with genomes of RNA, or RNA-DNA hybrid, or DNA with an RNA replication intermediate.(30,45,47) The 858 M.”
BackgroundAn updated structural classification of replicative DNA polymerases
Raia, P., Delarue, M. H., & Sauguet, L. (2019) · Biochemical Society Transactions · doi:10.1042/bst20180579 · Cited by 49
Anantharaman, V., Iyer, L. M., & Aravind, L. (2010) · Biology Direct · doi:10.1186/1745-6150-5-43 · Cited by 51
“Given that certain reconstructions of LUCA posit a notable role for RNA-based genetic material [23], it is possible that this ancestral enzyme might have had a prominent role in LUCA as an enzyme that repaired RNA through its polymerase or nucleotidyltransferase activity.”
BackgroundSelf-citationEchoes from the past – are we still in an RNP world?
Brosius, J. (2005) · Cytogenetic and Genome Research · doi:10.1159/000084934 · Cited by 48
“The enzyme gradually converted RNA genomes into DNA genomes (Brosius, 1999d; Leipe et al., 1999).”
BackgroundDNA repair in hyperthermophilic and hyperradioresistant microorganisms
Ishino, Y., & Narumi, I. (2015) · Current Opinion in Microbiology · doi:10.1016/j.mib.2015.05.010 · Cited by 49
Did group II intron proliferation in an endosymbiont-bearing archaeon create eukaryotes?
Poole, A. M. (2006) · Biology Direct · doi:10.1186/1745-6150-1-36 · Cited by 48
“It is likewise accepted that there are numerous similarities between archaea and eukaryotes [18] – eukaryote-like histones have been found in both euryarchaea and crenarchaea [19]; archaea and eukaryotes make use of small RNAs (known as small nucleolar or snoRNAs in eukaryotes) to guide ribose methylation and pseudour…”
BackgroundA proposal: Evolution of PCNA's role as a marker of newly replicated DNA
Georgescu, R. E., Langston, L. D., & O’Donnell, M. E. (2015) · DNA repair · doi:10.1016/j.dnarep.2015.01.015 · Cited by 48
“While most information transfer processes, such as transcription and translation, are performed by enzymes that share homology in cells from all domains of life, comparative genomics reveals the surprising finding that the core enzymes of DNA replication: polymerases, helicase, primase, and ssDNA binding proteins, sha…”
BackgroundInfluentialGenome size evolution in the Archaea
Kellner, S., Spang, A., Offre, P., Szöllősi, G. J., Petitjean, C., & Williams, T. A. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20180021 · Cited by 49
Origin and Evolution of DNA and DNA Replication Machineries
Forterre, P., Filée, J., & Myllykallio, H. (2007) · Springer eBooks · doi:10.1007/0-387-26887-1_10 · Cited by 47
The late appearance of DNA, the nature of the LUCA and ancestors of the domains of life
Giulio, M. D. (2020) · Biosystems · doi:10.1016/j.biosystems.2020.104330 · Cited by 48
Genomics and early cellular evolution. The origin of the DNA world
Forterre, P. (2001) · Comptes Rendus de l Académie des Sciences - Series III - Sciences de la Vie · doi:10.1016/s0764-4469(01)01403-2 · Cited by 46
Why Are There So Many Diverse Replication Machineries?
Forterre, P. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.09.032 · Cited by 46
Luca : À la recherche du plus proche ancêtre commun universel
Forterre, P., Gribaldo, S., & Brochier‐Armanet, C. (2005) · médecine/sciences · doi:10.1051/medsci/20052110860 · Cited by 46
“Pour expliquer la présence, dans la liste des protéines universelles, des ARN polymérases impliquées dans la transcription de l’ADN et de quelques protéines 3R, Koonin et ses collaborateurs ont proposé un Luca dont le génome était composé d’ARN, mais qui contenait déjà de l’ADN répliqué par rétrotranscription [10] : c…”
BackgroundElaborated Action of the Human Primosome
Baranovskiy, A. G., & Tahirov, T. H. (2017) · Genes · doi:10.3390/genes8020062 · Cited by 43
“Eukaryotic and archaeal primases have a similar structural organization, which indicates a common evolutionary ancestor [29].”
BackgroundDaimon, K., Kawarabayasi, Y., Kikuchi, H., Sako, Y., & Ishino, Y. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.3.687-694.2002 · Cited by 44
“In addition, after the total genome sequences of several archaeal organisms were determined, it was confirmed that several genes encoding proteins sharing sequence similarities with eukaryotic DNA replication proteins are present in all archaeal genomes (5, 10, 15, 32).”
BackgroundKähler, M., & Antranikian, G. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.3.655-663.2000 · Cited by 44
Starkuviene, V. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.10.2097 · Cited by 43
Carl Woese's vision of cellular evolution and the domains of life
Koonin, E. V. (2014) · RNA Biology · doi:10.4161/rna.27673 · Cited by 41
“Thus, under the symbiogenetic scenario for the origin of eukaryotes, there are two basic cell types, archaeal and bacterial, which differ in many fundamental features, above all, the structure and biogenesis of the cell membranes and the organization and origin of the DNA replication machinery.(61,62) These major diff…”
Self-citationMerhej, V., & Raoult, D. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00113 · Cited by 42
“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).”
BackgroundHaloferax volcanii —a model archaeon for studying DNA replication and repair
Pérez-Arnaiz, P., Dattani, A., Smith, V., & Allers, T. (2020) · Open Biology · doi:10.1098/rsob.200293 · Cited by 46
The Evolutionary History of the Translation Machinery
Fox, G. E., & Naik, A. K. (2007) · Springer eBooks · doi:10.1007/0-387-26887-1_6 · Cited by 42
The Eukaryotic Replication Machine
Zhang, D., & O’Donnell, M. E. (2016) · The Enzymes · doi:10.1016/bs.enz.2016.03.004 · Cited by 39
Rapid progress of DNA replication studies in Archaea, the third domain of life
Ishino, Y., & Ishino, S. (2012) · Science China Life Sciences · doi:10.1007/s11427-012-4324-9 · Cited by 39
Giraldo, R., & Díaz‐Orejas, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.081079298 · Cited by 39
Koonin, E. V. (2014) · Antonie van Leeuwenhoek · doi:10.1007/s10482-014-0169-5 · Cited by 34
“(i) did not have a typical, large DNA genome (Forterre 2006; Leipe et al. 1999) and/or.”
BackgroundMethodInfluentialSelf-citationAravind, L., Iyer, L. M., & Burroughs, A. M. (2022) · Annual Review of Biomedical Data Science · doi:10.1146/annurev-biodatasci-122220-101119 · Cited by 40
Self-citationEgel, R., & Penny, D. (2007) · Genome dynamics and stability · doi:10.1007/7050_2007_036 · Cited by 40
“This reservation is based on the disturbing absence of homology of the replicative DNA polymerases in bacteria and archaea/eukaryotes ( Leipe et al. 1999 ).”
BackgroundWitzany, G. (2008) · Biosemiotics · doi:10.1007/s12304-008-9018-0 · Cited by 39
“Recent research suggests thinking about the early stages of life as a pre-cellular RNA gene pool with RNA viruses, retroviruses and—by reverse transcriptase of singlestranded RNA viral genomes—also double-stranded DNA viruses (Leipe et al. 1999; Martin 2005; Koonin et al. 2006; Brosius 2003; Flavell 1995).”
BackgroundMatsunaga, F., Glatigny, A., Mucchielli-Giorgi, M.-H., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm212 · Cited by 38
Extra-chromosomal elements and the evolution of cellular DNA replication machineries
McGeoch, A. T., & Bell, S. D. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2426 · Cited by 37
“This mechanistic framework is shared by all cellular organisms, so it is truly remarkable that the protein machinery that bacteria use to replicate their genomes is not directly related, at the primary sequence level, to the machinery that is present in archaea and eukaryote”
BackgroundKeppetipola, N., & Shuman, S. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.20.6902-6908.2005 · Cited by 37
“A common ancestry for archaea and eucarya is supported by the similarities in their DNA replication machineries, which differ from those of bacteria (2, 11 ).”
BackgroundArchaeal DNA replication: spotlight on a rapidly moving field
Bohlke, K., Pisani, F. M., Rossi, M., & Antranikian, G. (2002) · Extremophiles · doi:10.1007/s007920100222 · Cited by 36
“The replicational cycle of the LUCA was proposed to be mirrored in today’s retroid viruses, especially caulimoviruses and hepadnaviruses (Leipe et al. 1999).”
Displacement of the canonical single-stranded DNA-binding protein in the Thermoproteales
Paytubi, S., McMahon, S. A., Graham, S., Liu, H., Botting, C. H., Makarova, K. S., Koonin, E. V., Naismith, J. H., & White, M. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113277108 · Cited by 35
“Nonorthologous gene displacement is a common phenomenon in genome evolution that encompasses even central cellular functions, in particular key components of the DNA replication machinery (35).”
BackgroundSelf-citationIntermolecular ion pairs maintain the toroidal structure of Pyrococcus furiosus PCNA
Matsumiya, S., Ishino, S., Ishino, Y., et al. (2003) · Protein Science · doi:10.1110/ps.0234503 · Cited by 36
“Copyright © 2003 The Protein Society 823 viewed for DNA replication in Edgell and Doolittle 1997; Ishino and Cann 1998; Cann and Ishino 1999; Leipe et al. 1999).”
Geibel, S., Banchenko, S., Engel, M., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902910106 · Cited by 35
“S1 B and C and S5), RepB is apparently the prototype of a distinct class of primases (36) with high sequence homology and exclusive leading-strand replication mode.”
BackgroundEvolution of Genes and Organisms
Olendzenski, L., & Gogarten, J. P. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04998.x · Cited by 38
Replisome structure and conformational dynamics underlie fork progression past obstacles
Yao, N. Y., & O’Donnell, M. E. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.02.008 · Cited by 33
“Structure of C-family polymerases Bacterial replicases are large DNA polymerases that constitute a unique family referred to as the C-family [13].”
BackgroundInfluentialValas, R. E., & Bourne, P. E. (2011) · Biology Direct · doi:10.1186/1745-6150-6-16 · Cited by 35
“Third, the DNA replication machinery of these two superkingdoms is very different; many key proteins comprising this machinery have a superkingdom specific distribution [4].”
BackgroundInfluentialVoter, A. F., Killoran, M. P., Ananiev, G. E., Wildman, S. A., Hoffmann, F. M., & Keck, J. L. (2017) · SLAS DISCOVERY · doi:10.1177/2472555217712001 · Cited by 32
“The molecular machinery essential for bacterial replication and genome maintenance is surprisingly dissimilar from analogous proteins in eukaryotes, so much so that it is thought that processes such as replication could have evolved independently.(7) From a therapeutic perspective, this difference makes genome mainten…”
BackgroundAnalyzing the symmetrical arrangement of structural repeats in proteins with CE-Symm
Bliven, S. E., Lafita, A., Rose, P. W., Capitani, G., Prlić, A., & Bourne, P. E. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006842 · Cited by 33
“As a historical note, the homology between bacterial and eurkaryotic DNA clamps was only acknowledged when the structures were solved and the similarity of their complexes was identified [41].”
BackgroundAn Evolutionary Analysis of Lateral Gene Transfer in Thymidylate Synthase Enzymes
Stern, A., Mayrose, I., Penn, O., Shaul, S., Gophna, U., & Pupko, T. (2010) · Systematic Biology · doi:10.1093/sysbio/syp104 · Cited by 31
“…encoding ThyA and ThyX may shed light on the actively debated wider issue regarding the origins of viral and cellular DNA (Hendrix et al. 1999; Leipe et al. 1999; Villarreal and DeFilippis 2000; Bell 2001; Forterre 2002; Bamford 2003; Filee et al. 2003; Forterre 2005; Koonin and Martin 2005;…”
BackgroundDistinct Double- and Single-Stranded DNA Binding of E. coli Replicative DNA Polymerase III α Subunit
McCauley, M. J., Shokri, L., Sefcikova, J., et al. (2008) · ACS Chemical Biology · doi:10.1021/cb8001107 · Cited by 32
“ment with other observations (7), suggests that the OB-”
Eukaryotic/Archaeal Primase and MCM Proteins Encoded in a Bacteriophage Genome
McGeoch, A. T., & Bell, S. D. (2005) · Cell · doi:10.1016/j.cell.2004.11.031 · Cited by 31
Jokela, M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh558 · Cited by 31
“It has been proposed that the modern-type system for double-stranded DNA replication likely evolved independently in the bacterial and archaeal/eukaryotic lineages (37).”
BackgroundAlley, S. C., Trakselis, M. A., Mayer, M. U., Ishmael, F. T., Jones, A. D., & Benkovic, S. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104956200 · Cited by 31
Bacterial and Eukaryotic Replisome Machines.
Yao, N. Y., & O’Donnell, M. E. (2016) · PubMed · Cited by 29
Tori, K., Kimizu, M., Ishino, S., et al. (2007) · Journal of Bacteriology · doi:10.1128/jb.00073-07 · Cited by 30
“Biochemical research efforts have suggested that the principle of the DNA replication mechanism seems to be the same in the three biological domains, Bacteria, Eukarya, and Archaea (6, 10, 11, 19), although the protein factors with conserved functions are predicted to have evolved from different origins based on the d…”
BackgroundThe Use of Phylogenetic Profiles for Gene Predictions
Liberles, D. A., Thoren, A., von HEIJNE, G., et al. (2002) · Current Genomics · doi:10.2174/1389202023350499 · Cited by 30
“It has been suggested [ 22 ] that DNA replication has evolved at least twice independently and that the last common ancestor of Bacteria and Eukaryota/Archea had a genetic system that contained RNA and DNA, with the latter produced by reverse transcription only.”
MethodDistinctive activities of DNA polymerases during human DNA replication
Rytkönen, A. K., Vaara, M., Nethanel, T., Kaufmann, G., Sormunen, R. T., Läärä, E., Nasheuer, H., Rahmeh, A. A., Lee, M., Syväoja, J. E., et al. (2006) · FEBS Journal · doi:10.1111/j.1742-4658.2006.05310.x · Cited by 29
Structural analysis of polarizing indels: an emerging consensus on the root of the tree of life
Valas, R. E., & Bourne, P. E. (2009) · Biology Direct · doi:10.1186/1745-6150-4-30 · Cited by 28
The Landscape of the Emergence of Life
Jheeta, S. (2017) · Life · doi:10.3390/life7020027 · Cited by 28
“, it possessed a functional ribosome of some kind [8].”
BackgroundReplisome dynamics and use of DNA trombone loops to bypass replication blocks
Yao, N. Y., & O’Donnell, M. E. (2008) · Molecular BioSystems · doi:10.1039/b811097b · Cited by 30
Yadav, A. K., & Polášek-Sedláčková, H. (2024) · Communications Biology · doi:10.1038/s42003-024-05855-w · Cited by 28
Nasir, A., Kim, K. M., & Caetano‐Anollés, G. (2014) · Archaea · doi:10.1155/2014/706468 · Cited by 27
Nuutinen, T., Tossavainen, H., Fredriksson, K., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn497 · Cited by 27
“Early cellular evolution was accompanied by gross genetic rearrangements (1–3), which resulted in apparentmodularity of proteins (4) and in unexpected structural similarities and dissimilarities among cellular forms of life (5,6).”
BackgroundStructural Mechanisms of Hexameric Helicase Loading, Assembly, and Unwinding
Trakselis, M. A. (2016) · F1000Research · doi:10.12688/f1000research.7509.1 · Cited by 27
The Origin(s) of Cell(s): Pre-Darwinian Evolution from FUCAs to LUCA
Tang, S. (2021) · Journal of Molecular Evolution · doi:10.1007/s00239-021-10014-4 · Cited by 26
Gutiérrez, R. M., Blanco, E. L., & Aranguren, Y. (2020) · Saudi Journal of Biological Sciences · doi:10.1016/j.sjbs.2020.06.015 · Cited by 26
Sawai, H., Nagashima, J.-I., Kuwahara, M., et al. (2007) · Chemistry & Biodiversity · doi:10.1002/cbdv.200790165 · Cited by 26
Ishino, Y., Tsurimoto, T., Ishino, S., et al. (2001) · Genes to Cells · doi:10.1046/j.1365-2443.2001.00451.x · Cited by 26
“Specifically, several genes encoding proteins sharing sequence similarities with eukaryotic DNA replication proteins are present in all archaeal genomes sequenced to date (reviewed in Edgell & Doolittle 1997; Ishino & Cann 1998; Leipe et al. 1999), and some of the gene products have been characterized biochemically (r…”
BackgroundArchitecture of the Saccharomyces cerevisiae Replisome
Bai, L., Yuan, Z., Sun, J., Georgescu, R. E., O’Donnell, M. E., & Li, H. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-6955-0_10 · Cited by 25
“Many key replication proteins, such as the replicative helicase, DNA polymerases, primase, and single strand binding protein, are evolutionarily unrelated between bacteria and archaea/eukarya (Forterre et al. 2004; Leipe et al. 1999).”
BackgroundBoudet, J., Devillier, J.-C., Wiegand, T., Salmon, L., Meier, B. H., Lipps, G., & Allain, F. H. ‐. (2018) · Cell · doi:10.1016/j.cell.2018.11.031 · Cited by 25
Evolution of reduced prokaryotic genomes and the minimal cell concept: Variations on a theme
Delaye, L., & Moyá, A. (2010) · BioEssays · doi:10.1002/bies.200900161 · Cited by 25
“Despite controversies regarding the chemical nature of the genome of the LCA,((38)) the similarities of DNA replication among cells and the homology between certain components of the DNA replication machinery((39)) suggest that DNA-based genomes may have evolved prior to the existence of the LCA.”
Lifeness signatures and the roots of the tree of life
Malaterre, C. (2010) · Biology & Philosophy · doi:10.1007/s10539-010-9220-8 · Cited by 29
“For some, these genes would be made out of DNA (Forterre 2002; Dworkin et al. 2003); others favor a mixed RNA-DNA genome and replication system (Leipe et al. 1999).”
BackgroundThe Case for an Early Biological Origin of DNA
Poole, A. M., Horinouchi, N., Catchpole, R. J., Si, D., Hibi, M., Tanaka, K., & Ogawa, J. (2014) · Journal of Molecular Evolution · doi:10.1007/s00239-014-9656-6 · Cited by 26
“Consequently, it is difficult to place any complete DNA-associated processes in the LUCA (Forterre et al. 2004; Harris et al. 2003; Leipe et al. 1999).”
BackgroundMethodInfluentialPonomarev, V. A., Makarova, K. S., Aravind, L., & Koonin, E. V. (2003) · Microbial Physiology · doi:10.1159/000071074 · Cited by 24
“Many of the central components of the DNA replication machineries in the bacterial and in the archaeoeukaryotic lineage are either unrelated or only distantly related to each other [Edgell and Doolittle, 1997; Leipe et al., 1999].”
BackgroundSelf-citationBacterial homologs of the small subunit of eukaryotic DNA primase.
Ev, K., Yi, W., As, K., et al. (2000) · PubMed · Cited by 24
Self-citationKinetics and Fidelity of Polymerization by DNA Polymerase III from Sulfolobus solfataricus
Bauer, R. J., Begley, M. T., & Trakselis, M. A. (2012) · Biochemistry · doi:10.1021/bi201799a · Cited by 23
The Last Universal Common Ancestor of Ribosome-Encoding Organisms: Portrait of LUCA
Forterre, P. (2024) · Journal of Molecular Evolution · doi:10.1007/s00239-024-10186-9 · Cited by 27
“The RNA-LUCA hypothesis has sometimes been refuted because the set of universal protein includes a few proteins involved in DNA metabolism or in the synthesis of DNA precursors (dNTPs) (Leipe et al. 1999, Becerra et al. 2007a, Cantine and Fournier 2018, Koonin et al. 2020).”
Is it possible that cells have had more than one origin?
de Farías, S. T., José, M. V., & Prosdocimi, F. (2021) · Biosystems · doi:10.1016/j.biosystems.2021.104371 · Cited by 23
The Nature of the Last Common Ancestor
Delaye, L., Becerra, A., & Lazcano, A. (2004) · Springer eBooks · doi:10.1007/0-387-26887-1_3 · Cited by 23
Distinct co-evolution patterns of genes associated to DNA polymerase III DnaE and PolC
Engelen, S., Vallenet, D., Médigue, C., & Danchin, A. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-69 · Cited by 24
“Our observations are consistent with the discovery of DNA and DNA replication at least twice [66] suggesting that the origin of present living organisms was a community of organisms developing more or less independently from one another (the progenote hypothesis [67,68]), splitting and fusing as time elapsed until the…”
Result
Metadata
- Authors
- Leipe, D. D., Aravind, L., & Koonin, E. V.
- Affiliations
- National Institutes of Health (US)
- Texas A&M University (US)
- Corresponding author
- Koonin, E. V.
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 1999-09-01
- Volume
- 27
- Issue
- 17
- Pages
- 3389-3401
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC148579
- OpenAlex
- W2018024025
- Semantic Scholar
- 9f9be31d2a06621cfbcaa7642db469b8cea929dc
- Cited by
- 351
- References
- 66
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 16 · 2023: 5 · 2022: 5 · 2021: 11 · 2020: 10 · 2019: 6 · 2018: 12 · 2017: 13 · 2016: 15 · 2015: 13 · 2014: 18 · 2013: 12 · 2012: 5
- FWCI
- 13.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nucleic Acids Research (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- DNA replication, origin of replication, convergent evolution, last common ancestor, primase, replicative helicase, proofreading exonuclease, DNA ligase, RNA-DNA hybrids, reverse transcription, sequence conservation
- MeSH terms
- Animals, Bacterial Proteins, Cytoplasm, DNA Replication, Drosophila, Fungal Proteins, Models, Genetic, Sequence Homology, Nucleic Acid, Databases, Factual, Sequence Analysis, DNA, Evolution, Molecular, Archaeal Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review