Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes
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BACKGROUND: Comparative analysis of sequenced genomes reveals numerous instances of apparent horizontal gene transfer (HGT), at least in prokaryotes, and indicates that lineage-specific gene loss might have been even more common in evolution. This complicates the notion of a species tree, which needs to be re-interpreted as a prevailing evolutionary trend, rather than the full depiction of evolution, and makes reconstruction of ancestral genomes a non-trivial task. RESULTS: We addressed the problem of constructing parsimonious scenarios for individual sets of orthologous genes given a species tree. The orthologous sets were taken from the database of Clusters of Orthologous Groups of proteins (COGs). We show that the phyletic patterns (patterns of presence-absence in completely sequenced genomes) of almost 90% of the COGs are inconsistent with the hypothetical species tree. Algorithms were developed to reconcile the phyletic patterns with the species tree by postulating gene loss, COG emergence and HGT (the latter two classes of events were collectively treated as gene gains). We prove that each of these algorithms produces a parsimonious evolutionary scenario, which can be represented as mapping of loss and gain events on the species tree. The distribution of the evolutionary events among the tree nodes substantially depends on the underlying assumptions of the reconciliation algorithm, e.g. whether or not independent gene gains (gain after loss after gain) are permitted. Biological considerations suggest that, on average, gene loss might be a more likely event than gene gain. Therefore different gain penalties were used and the resulting series of reconstructed gene sets for the last universal common ancestor (LUCA) of the extant life forms were analysed. The number of genes in the reconstructed LUCA gene sets grows as the gain penalty increases. However, qualitative examination of the LUCA versions reconstructed with different gain penalties indicates that, even with a gain penalty of 1 (equal weights assigned to a gain and a loss), the set of 572 genes assigned to LUCA might be nearly sufficient to sustain a functioning organism. Under this gain penalty value, the numbers of horizontal gene transfer and gene loss events are nearly identical. This result holds true for two alternative topologies of the species tree and even under random shuffling of the tree. Therefore, the results seem to be compatible with approximately equal likelihoods of HGT and gene loss in the evolution of prokaryotes. CONCLUSIONS: The notion that gene loss and HGT are major aspects of prokaryotic evolution was supported by quantitative analysis of the mapping of the phyletic patterns of COGs onto a hypothetical species tree. Algorithms were developed for constructing parsimonious evolutionary scenarios, which include gene loss and gain events, for orthologous gene sets, given a species tree. This analysis shows, contrary to expectations, that the number of predicted HGT events that occurred during the evolution of prokaryotes might be approximately the same as the number of gene losses. The approach to the reconstruction of evolutionary scenarios employed here is conservative with regard to the detection of HGT because only patterns of gene presence-absence in sequenced genomes are taken into account. In reality, horizontal transfer might have contributed to the evolution of many other genes also, which makes it a dominant force in prokaryotic evolution.
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LUCA may have had a genome of as many as 600 genes, with the suggested set nearly sufficient to sustain an organism.
“Analysis of the distribution of conserved genes indicates that LUCA may have had a genome of as many as 600 genes, with the suggested set again nearly sufficient to sustain an organism (Mirkin et al. 2003).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Mirkin et al. 2003
There is good evidence that LUCA's genome was small but functionally fairly comprehensive.
“However, there is good evidence that LUCA's genome was small but functionally fairly comprehensive (Mirkin et al. 2003;Ranea et al. 2006;Koonin 2003).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Mirkin et al. 2003
The pre-LUCA histories of some gene families can be examined.
“However, the pre-LUCA histories of some gene families can be examined (eg., Mirkin et al. 2003;Ranea et al. 2006;Gogarten and Taiz 1992;Fournier et al. 2015a;Fournier et al. 2015b).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Mirkin et al. 2003
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Cites
Molecular Evolution and Phylogenetics
Nei, M., & Kumar, S. (2000) · doi:10.1093/oso/9780195135848.001.0001 · Cited by 8,012 · see citing works
Toward Defining the Course of Evolution: Minimum Change for a Specific Tree Topology
Fitch, W. M. (1971) · Systematic Biology · doi:10.1093/sysbio/20.4.406 · Cited by 7,690 · see citing works
Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
Woese, C. R., Kandler, O., & Wheelis, M. L. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.12.4576 · Cited by 6,128 · see citing works
Toward Defining the Course of Evolution: Minimum Change for a Specific Tree Topology
Fitch, W. M. (1971) · Systematic Zoology · doi:10.2307/2412116 · Cited by 5,661 · see citing works
Woese, C. R. (1987) · Microbiological Reviews · doi:10.1128/mr.51.2.221-271.1987 · Cited by 5,042 · see citing works
A Genomic Perspective on Protein Families
Tatusov, R. L., Koonin, E. V., & Lipman, D. J. (1997) · Science · doi:10.1126/science.278.5338.631 · Cited by 3,552 · see citing works
Self-citationTime Warps, String Edits, and Macromolecules: The Theory and Practice of Sequence Comparison
Sankoff, D., & Kruskal, J. B. (1983) · Medical Entomology and Zoology · Cited by 1,940 · see citing works
Phylogenetic Classification and the Universal Tree
Doolittle, W. F. (1999) · Science · doi:10.1126/science.284.5423.2124 · Cited by 1,888 · see citing works
The COG database: new developments in phylogenetic classification of proteins from complete genomes
Tatusov, R. L. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.1.22 · Cited by 1,873 · see citing works
Nelson, K. E., Clayton, R. A., Gill, S. R., Gwinn, M. L., Dodson, R. J., Haft, D. H., Hickey, E. K., Peterson, J. D., Nelson, W. C., Ketchum, K. A., et al. (1999) · Nature · doi:10.1038/20601 · Cited by 1,493 · see citing works
Molecular Systematics: 1994–1995
Sytsma, K. J., & Hahn, W. J. (1997) · Springer eBooks · doi:10.1007/978-3-642-60458-4_21 · Cited by 1,173 · see citing works
Classification and evolution of P-loop GTPases and related ATPases
Leipe, D. D., Wolf, Y. I., Koonin, E. V., & Aravind, L. (2002) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.5378 · Cited by 1,148 · see citing works
Self-citationHorizontal gene transfer in prokaryotes: Quantification and classification
Koonin, E. V., Makarova, K. S., & Aravind, L. (2001) · Annual Review of Microbiology · doi:10.1146/annurev.micro.55.1.709 · Cited by 1,126 · see citing works
Self-citationConservation 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 1,037 · see citing works
Prokaryotic Evolution in Light of Gene Transfer
Gogarten, J. P., Doolittle, W. F., & Lawrence, J. G. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004046 · Cited by 986 · see citing works
The winds of (evolutionary) change: breathing new life into microbiology
Olsen, G. J., Woese, C. R., & Overbeek, R. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.1.1-6.1994 · Cited by 904 · see citing works
Iwabe, N., Kuma, K., Hasegawa, M., Osawa, S., & Miyata, T. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.23.9355 · Cited by 902 · see citing works
Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes.
Gogarten, J. P., Kibak, H., Dittrich, P., Taiz, L., Bowman, E. J., Bowman, B. J., Manolson, M. F., Poole, R. J., Date, T., Oshima, T., et al. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.17.6661 · Cited by 781 · see citing works
Genome phylogeny based on gene content
Snel, ., Peer Bork, B., & Huynen, M. A. (1999) · Nature Genetics · doi:10.1038/5052 · Cited by 708 · see citing works
Aminoacyl-tRNA Synthetases, the Genetic Code, and the Evolutionary Process
Woese, C. R., Olsen, G. J., Ibba, M., & Söll, D. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.1.202-236.2000 · Cited by 706 · see citing works
Reconstructing ancestral character states under Wagner parsimony
Swofford, D. L., & Maddison, W. P. (1987) · Mathematical Biosciences · doi:10.1016/0025-5564(87)90074-5 · Cited by 593 · see citing works
Minimal Mutation Trees of Sequences
Sankoff, D. (1975) · SIAM Journal on Applied Mathematics · doi:10.1137/0128004 · Cited by 579 · see citing works
Page, R. (1994) · Systematic Biology · doi:10.1093/sysbio/43.1.58 · Cited by 526 · see citing works
Archaea and the prokaryote-to-eukaryote transition
Brown, J. R., & Doolittle, W. F. (1997) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.61.4.456-502.1997 · Cited by 485 · see citing works
Mechanisms of Evolution in Rickettsia conorii and R. prowazekii
Ogata, H., Audic, S., Renesto, P., Fournier, P., Barbe, V., Samson, D. S., Roux, V., Cossart, P., Weissenbach, J., Claverie, J., et al. (2001) · Science · doi:10.1126/science.1061471 · Cited by 419 · see citing works
Wolf, Y. I., Aravind, L., Grishin, N. V., & Koonin, E. V. (1999) · Genome Research · doi:10.1101/gr.9.8.689 · Cited by 410 · see citing works
Self-citationPhylogenetic Analysis Under Dollo's Law
Farris, J. S. (1977) · Systematic Biology · doi:10.1093/sysbio/26.1.77 · Cited by 394 · see citing works
Universal trees based on large combined protein sequence data sets
Brown, J. R., Douady, C. J., Italia, M. J., Marshall, W. E., & Stanhope, M. J. (2001) · Nature Genetics · doi:10.1038/90129 · Cited by 381 · see citing works
Genome trees and the tree of life
Wolf, Y. I., Rogozin, I. B., Grishin, N. V., & Koonin, E. V. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02744-0 · Cited by 362 · see citing works
Self-citationWolf, Y. I., Rogozin, I. B., Kondrashov, A. S., & Koonin, E. V. (2001) · Genome Research · doi:10.1101/gr.gr-1619r · Cited by 357 · see citing works
Self-citationDid DNA replication evolve twice independently?
Leipe, D. D., Aravind, L., & Koonin, E. V. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.17.3389 · Cited by 351 · cited 2× · see citing works
“This is likely to reflect radical innovation at these evolutionary junctures, perhaps including even independent origin of DNA replication systems [61,71,72].”
Self-citationGenomes in Flux: The Evolution of Archaeal and Proteobacterial Gene ContentPreprint
Snel, ., Bork, P., & Huynen, M. A. (2001) · Genome Research · doi:10.1101/gr.176501 · Cited by 351 · see citing works
How Many Genes Can Make a Cell: The Minimal-Gene-Set Concept
Koonin, E. V. (2000) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.1.1.99 · Cited by 336 · see citing works
Self-citationEvidence for massive gene exchange between archaeal and bacterial hyperthermophiles
Aravind, L., Tatusov, R. L., Wolf, Y. I., Walker, D. R., & Koonin, E. V. (1998) · Trends in Genetics · doi:10.1016/s0168-9525(98)01553-4 · Cited by 333 · see citing works
Self-citationSystematics, historical ecology, and North American freshwater fishes
Howe, J. C. (1993) · Fisheries Research · doi:10.1016/0165-7836(93)90165-4 · Cited by 318 · see citing works
Koonin, E. V., Mushegian, A. R., Galperin, M. Y., & Walker, D. R. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.4821861.x · Cited by 310 · see citing works
Self-citationWhole genome-based phylogenetic analysis of free-living microorganisms
Gibbon, S. T. F., & House, C. H. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.21.4218 · Cited by 307 · see citing works
Genome trees constructed using five different approaches suggest new major bacterial clades
Wolf, Y. I., Rogozin, I. B., Grishin, N. V., Tatusov, R. L., & Koonin, E. V. (2001) · BMC Evolutionary Biology · doi:10.1186/1471-2148-1-8 · Cited by 304 · see citing works
Self-citationThe process of genome shrinkage in the obligate symbiont Buchnera aphidicola
Moran, N., & Mira, A. (2001) · Genome Biology · doi:10.1186/gb-2001-2-12-research0054 · Cited by 297 · see citing works
Phylogenetic Analysis Under Dollo's Law
Farris, J. S. (1977) · Systematic Zoology · doi:10.2307/2412867 · Cited by 291 · see citing works
Sequence ― Evolution ― Function: Computational Approaches in Comparative Genomics
Koonin, E. V., & Galperin, M. Y. (2010) · Cited by 283 · see citing works
Self-citationMinimum Mutation Fits to a Given Tree
Hartigan, J. A. (1973) · Biometrics · doi:10.2307/2529676 · Cited by 280 · see citing works
Systematics, Historical Ecology, and North American Freshwater Fishes.
Collette, B. B., & Mayden, R. L. (1993) · Systematic Biology · doi:10.2307/2992474 · Cited by 277 · see citing works
Comparative analysis of the genomes of the bacteria Mycoplasma pneumoniae and Mycoplasma genitalium
Himmelreich, R., Plagens, H., Hilbert, H., Reiner, B., & Herrmann, R. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.4.701 · Cited by 261 · see citing works
Non-orthologous gene displacement
Koonin, E. V., Mushegian, A. R., & Peer Bork, B. (1996) · Trends in Genetics · doi:10.1016/s0168-9525(96)80003-5 · Cited by 251 · see citing works
Self-citationNon-orthologous gene displacement
Koonin, E. V. (1996) · Trends in Genetics · doi:10.1016/0168-9525(96)20010-1 · Cited by 250 · see citing works
Self-citationUniversally conserved translation initiation factors
Kyrpides, N. C., & Woese, C. R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.1.224 · Cited by 247 · see citing works
The Genomic Tree as Revealed from Whole Proteome ComparisonsPreprint
Tekaia, F., Lazcano, A., & Dujon, B. (1999) · Genome Research · doi:10.1101/gr.9.6.550 · Cited by 242 · see citing works
Reconstruction of Ancient Molecular Phylogeny
Guigó, R., Muchnik, I. B., & Smith, T. F. (1996) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.1996.0071 · Cited by 242 · see citing works
Horizontal transfer of ATPase genes — the tree of life becomes a net of life
Hilario, E., & Gogarten, J. P. (1993) · Biosystems · doi:10.1016/0303-2647(93)90038-e · Cited by 241 · see citing works
Doolittle, W. F. (1999) · Trends in Cell Biology · doi:10.1016/s0962-8924(99)01664-5 · Cited by 241 · see citing works
The origin of the eukaryotic cell.
Gupta, R. S., & Golding, G. B. (1996) · PubMed · Cited by 239 · see citing works
A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein
Forterre, P. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02650-1 · Cited by 228 · see citing works
The origin of the eukaryotic cell
Gupta, R. S., & Golding, G. B. (1996) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(96)20013-1 · Cited by 215 · see citing works
Gene order is not conserved in bacterial evolution
Mushegian, A. R., & Koonin, E. V. (1996) · Trends in Genetics · doi:10.1016/0168-9525(96)20006-x · Cited by 212 · see citing works
Self-citationSelfish operons and speciation by gene transfer
Lawrence, J. G. (1997) · Trends in Microbiology · doi:10.1016/s0966-842x(97)01110-4 · Cited by 210 · see citing works
Variation and Evolution of the Citric-Acid Cycle: A Genomic Perspective
Huynen, M. A., Dandekar, T., & Bork, P. (1999) · Trends in Microbiology · doi:10.1016/s0966-842x(99)01539-5 · Cited by 188 · see citing works
Archaeal Phylogeny Based on Ribosomal Proteins
Matte-Tailliez, O., Brochier‐Armanet, C., Forterre, P., & Philippe, H. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004122 · Cited by 180 · see citing works
SHOT: a web server for the construction of genome phylogenies
Korbel, J. O., Snel, ., Huynen, M. A., & Peer Bork, B. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(01)02597-5 · Cited by 178 · see citing works
On surrogate methods for detecting lateral gene transfer
Ragan, M. A. (2001) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2001.tb10755.x · Cited by 177 · see citing works
Protein-based phylogenies support a chimeric origin for the eukaryotic genome.
Golding, G. B., & Gupta, R. S. (1995) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040178 · Cited by 162 · see citing works
Lin, J., & Gerstein, M. (2000) · Genome Research · doi:10.1101/gr.10.6.808 · Cited by 161 · see citing works
Makarova, K. S., Ponomarev, V. A., & Koonin, E. V. (2001) · Genome biology · doi:10.1186/gb-2001-2-9-research0033 · Cited by 161 · see citing works
Self-citationCritical Issues in Bacterial Phylogeny
Gupta, R. S., & Griffiths, E. (2002) · Theoretical Population Biology · doi:10.1006/tpbi.2002.1589 · Cited by 158 · see citing works
Eubacterial phylogeny based on translational apparatus proteins
Brochier‐Armanet, C., Bapteste, E. P., Moreira, D., & Philippe, H. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(01)02522-7 · Cited by 157 · see citing works
Detection of lateral gene transfer among microbial genomes
Ragan, M. A. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00244-6 · Cited by 151 · see citing works
Trends in protein evolution inferred from sequence and structure analysis
Aravind, L., Mazumder, R., Vasudevan, S., & Koonin, E. V. (2002) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(02)00334-2 · Cited by 148 · see citing works
Self-citationGenome size reduction through multiple events of gene disintegration in Buchnera APS
Silva, F. J., Latorre, A., & Moyá, A. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02483-0 · Cited by 139 · see citing works
Orthologs, paralogs and genome comparisons
Gogarten, J. P., & Olendzenski, L. (1999) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(99)00029-5 · Cited by 134 · see citing works
On a Mirkin-Muchnik-Smith Conjecture for Comparing Molecular Phylogenies
Zhang, L. (1997) · Journal of Computational Biology · doi:10.1089/cmb.1997.4.177 · Cited by 132 · see citing works
Genome plasticity as a paradigm of eubacteria evolution
Watanabe, H., Mori, H., Itoh, T., & Gojobori, T. (1997) · Journal of Molecular Evolution · doi:10.1007/pl00000052 · Cited by 131 · see citing works
Doolittle, W. F. (1999) · PubMed · Cited by 129 · see citing works
The evolutionary history of ribosomal protein RpS14:
Brochier‐Armanet, C., Philippe, H., & Moreira, D. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02142-9 · Cited by 126 · see citing works
Genome Data Shake Tree of Life
Pennisi, E. (1998) · Science · doi:10.1126/science.280.5364.672 · Cited by 125 · see citing works
Crystal structure of reverse gyrase: insights into the positive supercoiling of DNA
Rodriguez, A. C., & Stock, D. (2002) · The EMBO Journal · doi:10.1093/emboj/21.3.418 · Cited by 120 · see citing works
Clarke, G. D., Beiko, R. G., Ragan, M. A., & Charlebois, R. L. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.8.2072-2080.2002 · Cited by 117 · see citing works
A Biologically Consistent Model for Comparing Molecular Phylogenies
Mirkin, B., Muchnik, I. B., & Smith, T. F. (1995) · Journal of Computational Biology · doi:10.1089/cmb.1995.2.493 · Cited by 98 · see citing works
Self-citationReconciled trees and incongruent gene and species trees
Page, R., & Charleston, M. (1997) · DIMACS series in discrete mathematics and theoretical computer science · doi:10.1090/dimacs/037/04 · Cited by 90 · see citing works
Is It Time to Uproot the Tree of Life?
Pennisi, E. (1999) · Science · doi:10.1126/science.284.5418.1305 · Cited by 89 · see citing works
Systematics, historical ecology and North American freshwater fishes
Greenwood, P. H. (1993) · Reviews in Fish Biology and Fisheries · doi:10.1007/bf00043387 · Cited by 81 · see citing works
Evolutionary anomalies among the aminoacyl-tRNA synthetases
Doolittle, R. F., & Handy, J. (1998) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(98)80030-0 · Cited by 78 · see citing works
Sequence — Evolution — Function
Koonin, E. V., & Galperin, M. Y. (2003) · Springer eBooks · doi:10.1007/978-1-4757-3783-7 · Cited by 76 · see citing works
Self-citationKurland, C. G. (2000) · EMBO Reports · doi:10.1093/embo-reports/kvd042 · Cited by 75 · see citing works
DNA Repair Systems in Archaea: Mementos from the Last Universal Common Ancestor?
DiRuggiero, J., Brown, J. R., Bogert, A. P., & Robb, F. T. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006570 · Cited by 67 · see citing works
The Last Universal Common Ancestor (LUCA), Simple or Complex?
Forterre, P., & Philippe, H. (1999) · Biological Bulletin · doi:10.2307/1542973 · Cited by 55 · see citing works
The universal ancestor was a thermophile or a hyperthermophile
Giulio, M. D. (2001) · Gene · doi:10.1016/s0378-1119(01)00781-8 · Cited by 53 · see citing works
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 · see citing works
Duplication-Based Measures of Difference Between Gene and Species Trees
Eulenstein, O., Mirkin, B., & Vingron, M. (1998) · Journal of Computational Biology · doi:10.1089/cmb.1998.5.135 · Cited by 43 · see citing works
Self-citationForterre, P., Benachenhou, N., & Labedan, B. (1993) · Nature · doi:10.1038/362795b0 · Cited by 21 · see citing works
On surrogate methods for detecting lateral gene transfer
Ragan, M. A. (2001) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(01)00262-2 · Cited by 17 · see citing works
The origin of the eukaryotic cell
Gupta, R. S. (1996) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(96)20013-1 · Cited by 16 · see citing works
Looking for the most “primitive” organism(s) on Earth today: the state of the art
Forterre, P. (1995) · Planetary and Space Science · doi:10.1016/0032-0633(94)00167-p · Cited by 13 · see citing works
Human chromosome 19 homologies.
Subramanian, S. (2001) · Genome biology · doi:10.1186/gb-2001-2-10-reports0033 · Cited by 10 · see citing works
Flagged first, then by citations
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Sorted by citations
Comparative genomics of the lactic acid bacteria.
Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V., Polouchine, N., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607117103 · Cited by 1,391 · see citing works
Self-citationOrthologs, Paralogs, and Evolutionary Genomics
Koonin, E. V. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.114725 · Cited by 1,323 · see citing works
Self-citationComparative genomics, minimal gene-sets and the last universal common ancestor
Koonin, E. V. (2003) · Nature Reviews Microbiology · doi:10.1038/nrmicro751 · Cited by 661 · see citing works
Self-citationGenomes in turmoil: quantification of genome dynamics in prokaryote supergenomes
Puigbò, P., Lobkovsky, A. E., Kristensen, D. M., Wolf, Y. I., & Koonin, E. V. (2014) · BMC Biology · doi:10.1186/s12915-014-0066-4 · Cited by 232 · see citing works
Self-citationBosi, E., Monk, J. M., Aziz, R. K., Fondi, M., Nizet, V., & Palsson, B. Ø. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523199113 · Cited by 266 · see citing works
Remnants of an Ancient Metabolism without Phosphate
Goldford, J. E., Hartman, H., Smith, T. F., & Segrè, D. (2017) · Cell · doi:10.1016/j.cell.2017.02.001 · Cited by 226 · see citing works
Koonin, E. V. (2016) · F1000Research · doi:10.12688/f1000research.8737.1 · Cited by 152 · see citing works
Self-citationPhylogenomic analysis of the GIY-YIG nuclease superfamily
Dunin-Horkawicz, S., Feder, M., & Bujnicki, J. M. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-98 · Cited by 133 · see citing works
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Martin, W. F., & Sousa, F. L. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018127 · Cited by 129 · see citing works
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Ranea, J. A. G., Sillero, A., Thornton, J. M., & Orengo, C. A. (2006) · Journal of Molecular Evolution · doi:10.1007/s00239-005-0289-7 · Cited by 122 · see citing works
Becerra, A., Delaye, L., Islas, S., & Lazcano, A. (2007) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.38.091206.095825 · Cited by 115 · see citing works
Parsons, C., Stüeken, E. E., Rosen, C. J., Mateos, K., & Anderson, R. E. (2021) · Geobiology · doi:10.1111/gbi.12419 · Cited by 91 · see citing works
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Xavier, J. C., Patil, K. R., & Rocha, I. (2014) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00050-13 · Cited by 58 · see citing works
LUCApedia: a database for the study of ancient life
Goldman, A. D., Bernhard, T. M., Dolzhenko, E., & Landweber, L. F. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1217 · Cited by 58 · see citing works
Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor
Cantine, M. D., & Fournier, G. P. (2018) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-017-9542-5 · Cited by 54 · see citing works
Scaling laws in enzyme function reveal a new kind of biochemical universality
Gagler, D. C., Karas, B., Kempes, C. P., Malloy, J., Mierzejewski, V., Goldman, A. D., Kim, H., & Walker, S. I. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2106655119 · Cited by 34 · see citing works
Kunnev, D., & Gospodinov, A. (2018) · Life · doi:10.3390/life8040044 · Cited by 24 · see citing works
- Authors
- Mirkin, B. G., Fenner, T. I., Galperin, M. Y., & Koonin, E. V.
- Affiliations
- University of London (GB)
- National Institutes of Health (US)
- Corresponding author
- Koonin, Eugene V
- Venue
- BMC Evolutionary Biology
- Published
- 2003-01-06
- Volume
- 3
- Issue
- 1
- Pages
- 2-2
- ISSN
- 1471-2148 (ISSN-L)
- PMC
- PMC149225
- OpenAlex
- W1483942228
- Cited by
- 368
- References
- 93
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 11 · 2023: 7 · 2022: 7 · 2021: 11 · 2020: 13 · 2019: 9 · 2018: 9 · 2017: 7 · 2016: 10 · 2015: 14 · 2014: 20 · 2013: 16 · 2012: 26
- FWCI
- 8.64
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMC Evolutionary Biology (publishedVersion)
- PubMed Central (publishedVersion, other-oa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Keywords
- horizontal gene transfer, gene loss, last universal common ancestor, ancestral genome reconstruction, orthologs, clusters of orthologous groups, prokaryotic evolution, genome evolution
- MeSH terms
- Algorithms, Amino Acid Sequence, Bacterial Proteins, Mathematical Computing, Models, Genetic, Molecular Sequence Data, Genome, Genome, Bacterial, Genome, Fungal, Gene Deletion, Evolution, Molecular, Computational Biology, Archaeal Proteins, Genome, Archaeal, Gene Transfer, Horizontal, Saccharomyces cerevisiae Proteins
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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.
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