E V Koonin
Affiliation: National Institutes of Health
- Koonin E. Hunting for Treasure Chests in Microbial Defense Islands. Mol Cell. 2018;70:761-762 pubmed publisher..A systematic strategy combining computation and experiment led to discovery of ten new defense systems that remain to be characterized mechanistically. ..
- Yutin N, Faure G, Koonin E, Mushegian A. Chordopoxvirus protein F12 implicated in enveloped virion morphogenesis is an inactivated DNA polymerase. Biol Direct. 2014;9:22 pubmed publisher..Thus, F12 appears to present a rare example of a drastic, exaptive functional change in virus evolution. This article was reviewed by Frank Eisenhaber and Juergen Brosius. ..
- Ibrahim B, Arkhipova K, Andeweg A, Posada Cespedes S, Enault F, Gruber A, et al. Bioinformatics Meets Virology: The European Virus Bioinformatics Center's Second Annual Meeting. Viruses. 2018;10: pubmed publisher..This report presents an overview of new developments and novel research findings that emerged during the meeting. ..
- Yutin N, Kapitonov V, Koonin E. A new family of hybrid virophages from an animal gut metagenome. Biol Direct. 2015;10:19 pubmed publisher..Virion proteins of mimiviruses were detected in the same metagenomes as the RVP suggesting that the virophages of the new family parasitize on giant viruses that infect protist inhabitants of the rumen. ..
- Shmakov S, Makarova K, Wolf Y, SEVERINOV K, Koonin E. Systematic prediction of genes functionally linked to CRISPR-Cas systems by gene neighborhood analysis. Proc Natl Acad Sci U S A. 2018;115:E5307-E5316 pubmed publisher..These predictions provide ample material for improving annotation of CRISPR-cas loci and experimental characterization of previously unsuspected aspects of CRISPR-Cas system functionality. ..
- Belinky F, Babenko V, Rogozin I, Koonin E. Purifying and positive selection in the evolution of stop codons. Sci Rep. 2018;8:9260 pubmed publisher..Although GC content has a major impact on stop codon frequencies, its contribution to the decreased frequency of UAA differs between bacteria and archaea, presumably, due to differences in their translation termination mechanisms. ..
- Koonin E, Makarova K, Zhang F. Diversity, classification and evolution of CRISPR-Cas systems. Curr Opin Microbiol. 2017;37:67-78 pubmed publisher..Comparative analysis of the effector complexes indicates that Class 2 systems evolved from mobile genetic elements on multiple, independent occasions. ..
- ..This direction of the information flow is likely to be one of the important routes of environment-genome interaction and could substantially contribute to the evolution of complex adaptive traits. ..
- Pagnier I, Yutin N, Croce O, Makarova K, Wolf Y, Benamar S, et al. Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae. Biol Direct. 2015;10:13 pubmed publisher..Characterization of B. massiliensis, a representative of a distinct bacterial phylum, thanks to its ability to grow in amoeba, reaffirms the critical role of diverse culture approaches in microbiology. ..
- Iranzo J, Lobkovsky A, Wolf Y, Koonin E. Immunity, suicide or both? Ecological determinants for the combined evolution of anti-pathogen defense systems. BMC Evol Biol. 2015;15:43 pubmed publisher..Some of the predictions of the model appear compatible with recent experimental evolution results and call for additional experiments. ..
- Chylinski K, Makarova K, Charpentier E, Koonin E. Classification and evolution of type II CRISPR-Cas systems. Nucleic Acids Res. 2014;42:6091-105 pubmed publisher..Distant homologs of Cas9 were identified among proteins encoded by diverse transposons, suggesting that type II CRISPR-Cas evolved via recombination of mobile nuclease genes with type I loci. ..
- Lobkovsky A, Wolf Y, Koonin E. Evolvability of an Optimal Recombination Rate. Genome Biol Evol. 2015;8:70-7 pubmed publisher..The predictions of the model were compatible with the observations on the dependence between genome rearrangement rate and gene flux in microbial genomes. ..
- Koonin E. On the origin of cells and viruses: primordial virus world scenario. Ann N Y Acad Sci. 2009;1178:47-64 pubmed publisher..The two surviving types of cellular life forms, archaea and bacteria, might have emerged from the LUCAS independently, along with, probably, numerous forms now extinct. ..
- Koonin E. Horizontal gene transfer: the path to maturity. Mol Microbiol. 2003;50:725-7 pubmed
- Yutin N, Bäckström D, Ettema T, Krupovic M, Koonin E. Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis. Virol J. 2018;15:67 pubmed publisher..From a supposedly minor group of bacterial and archaeal viruses, these viruses are emerging as a substantial component of the prokaryotic virome. ..
- Krupovic M, Dolja V, Koonin E. Plant viruses of the Amalgaviridae family evolved via recombination between viruses with double-stranded and negative-strand RNA genomes. Biol Direct. 2015;10:12 pubmed publisher..The chimeric genomes of amalgaviruses are a testament to the effectively limitless gene exchange between viruses that shaped the evolution of the virosphere. ..
- Koonin E. The Origin at 150: is a new evolutionary synthesis in sight?. Trends Genet. 2009;25:473-5 pubmed publisher..The hallmark of the Darwinian discourse of 2009 is the plurality of evolutionary processes and patterns. Nevertheless, glimpses of a new synthesis might be discernible in emerging universals of evolution. ..
- Kapitonov V, Makarova K, Koonin E. ISC, a Novel Group of Bacterial and Archaeal DNA Transposons That Encode Cas9 Homologs. J Bacteriol. 2015;198:797-807 pubmed publisher..Here, we describe in detail a novel family of transposable elements that encode the likely ancestors of Cas9 and outline the evolutionary scenario connecting different varieties of these transposons and Cas9. ..
- Koonin E. The wonder world of microbial viruses. Expert Rev Anti Infect Ther. 2010;8:1097-9 pubmed publisher..Viruses, in particular viruses that infect prokaryotes and unicellular eukaryotes, are emerging as the most abundant class of biological entities on earth and a major evolutionary and geochemical force. ..
- Koonin E. Towards a postmodern synthesis of evolutionary biology. Cell Cycle. 2009;8:799-800 pubmed..This expansion of evolutionary biology does not denigrate Darwin in the least but rather emphasizes the fertility of his ideas. ..
- Koonin E, Wolf Y. Just how Lamarckian is CRISPR-Cas immunity: the continuum of evolvability mechanisms. Biol Direct. 2016;11:9 pubmed publisher..These findings emphasize the continuity between random and directed mutations and the critical importance of evolved mechanisms that govern the mutational process. ..
- ..Combined with recent findings in prokaryotes, these results suggest that Lamarckian-type inheritance of acquired traits is a major evolutionary phenomenon. ..
- Krupovic M, Cvirkaite Krupovic V, Prangishvili D, Koonin E. Evolution of an archaeal virus nucleocapsid protein from the CRISPR-associated Cas4 nuclease. Biol Direct. 2015;10:65 pubmed publisher..To our knowledge, this is the first described case of exaptation of an enzyme for a virus capsid protein function. ..
- Koonin E, Wolf Y. The fundamental units, processes and patterns of evolution, and the tree of life conundrum. Biol Direct. 2009;4:33 pubmed publisher..This articles was reviewed by Valerian Dolja, W. Ford Doolittle, Nicholas Galtier, and William Martin. ..
- Galperin M, Makarova K, Wolf Y, Koonin E. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res. 2015;43:D261-9 pubmed publisher..The new version of the COGs is expected to become an important tool for microbial genomics. ..
- Yutin N, Koonin E. Pandoraviruses are highly derived phycodnaviruses. Biol Direct. 2013;8:25 pubmed publisher..We conclude that, despite their many unusual characteristics, Pandoraviruses are highly derived phycodnaviruses. These findings imply that giant viruses have independently evolved from smaller NCLDV on at least two occasions. ..
- Koonin E. Splendor and misery of adaptation, or the importance of neutral null for understanding evolution. BMC Biol. 2016;14:114 pubmed publisher..To claim adaptation, the neutral null has to be falsified. The adaptationist fallacy can be costly, inducing biologists to relentlessly seek function where there is none. ..
- Yutin N, Shevchenko S, Kapitonov V, Krupovic M, Koonin E. A novel group of diverse Polinton-like viruses discovered by metagenome analysis. BMC Biol. 2015;13:95 pubmed publisher..This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered. ..
- Koonin E. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 2010;11:209 pubmed publisher..Phylogenomics of eukaryote supergroups suggest a highly complex last common ancestor of eukaryotes and a key role of mitochondrial endosymbiosis in the origin of eukaryotes. ..
- Koonin E. New variants of known folds: do they bring new biology?. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2010;66:1226-9 pubmed publisher..These structures do not supplant direct biochemical experiments, but are indispensable for the complete characterization of proteins. ..
- Iranzo J, Cuesta J, Manrubia S, Katsnelson M, Koonin E. Disentangling the effects of selection and loss bias on gene dynamics. Proc Natl Acad Sci U S A. 2017;114:E5616-E5624 pubmed publisher..The horizontal gene transfer to loss ratio, but not duplication to loss ratio, correlates with genome size, potentially explaining increased abundance of neutral and costly elements in larger genomes. ..
- Omelchenko M, Makarova K, Wolf Y, Rogozin I, Koonin E. Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol. 2003;4:R55 pubmed..These findings also emphasize that not all aspects of operon evolution are selfish, with operon integrity maintained by purifying selection at the organism level. ..
- Koonin E. Darwinian evolution in the light of genomics. Nucleic Acids Res. 2009;37:1011-34 pubmed publisher..Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future. ..
- Koonin E, Wolf Y. Constraints and plasticity in genome and molecular-phenome evolution. Nat Rev Genet. 2010;11:487-98 pubmed publisher..Taken together, these findings are starting to reveal complex networks of evolutionary processes that must be integrated to attain a new synthesis of evolutionary biology. ..
- Koonin E. Taming of the shrewd: novel eukaryotic genes from RNA viruses. BMC Biol. 2010;8:2 pubmed publisher..The integrated copies could contribute to acquired immunity to the respective viruses. ..
- Iranzo J, Krupovic M, Koonin E. The Double-Stranded DNA Virosphere as a Modular Hierarchical Network of Gene Sharing. MBio. 2016;7: pubmed publisher..We formally identify a set of 14 viral hallmark genes that hold together the genomic network. ..
- Sela I, Wolf Y, Koonin E. Theory of prokaryotic genome evolution. Proc Natl Acad Sci U S A. 2016;113:11399-11407 pubmed..The tight spacing of protein-coding genes likely results from a combination of the deletion bias and purifying selection that efficiently eliminates nonfunctional, noncoding sequences. ..
- Rogozin I, Belinky F, Pavlenko V, Shabalina S, Kristensen D, Koonin E. Evolutionary switches between two serine codon sets are driven by selection. Proc Natl Acad Sci U S A. 2016;113:13109-13113 pubmed..The result is frequent reversal of amino acid replacements and, at short evolutionary distances, pervasive homoplasy. ..
- Kannan S, Rogozin I, Koonin E. MitoCOGs: clusters of orthologous genes from mitochondria and implications for the evolution of eukaryotes. BMC Evol Biol. 2014;14:237 pubmed publisher..The land plants are the only eukaryotic branch in which the gene transfer from the mitochondrial to the nuclear genome appears to be an active, ongoing process. ..
- Makarova K, Koonin E. Comparative genomics of Archaea: how much have we learned in six years, and what's next?. Genome Biol. 2003;4:115 pubmed..The majority of archaeal genes have not been experimentally characterized, but novel functional pathways have been predicted. ..
- Iranzo J, PuigbÃ² P, Lobkovsky A, Wolf Y, Koonin E. Inevitability of Genetic Parasites. Genome Biol Evol. 2016;8:2856-2869 pubmed..A numerical assessment of this hypothesis suggests that microbial populations cannot purge parasites while escaping Muller's ratchet. Thus, genetic parasites appear to be virtually inevitable in cellular organisms. ..
- Takeuchi N, Cordero O, Koonin E, Kaneko K. Gene-specific selective sweeps in bacteria and archaea caused by negative frequency-dependent selection. BMC Biol. 2015;13:20 pubmed publisher..Because many free-living prokaryotes are likely to evolve under NFDS caused by ubiquitous viruses, gene-specific selective sweeps driven by NFDS are expected to be a major, general phenomenon in prokaryotic populations. ..
- Koonin E. Preview. The incredible expanding ancestor of eukaryotes. Cell. 2010;140:606-8 pubmed publisher..The genome sequence of the amoeboflagellate Naegleria gruberi reported by Fritz-Laylin et al. (2010) reveals the surprising complexity of this unicellular organism and, by inference, of the last common eukaryotic ancestor. ..
- Kristensen D, Saeed U, Frishman D, Koonin E. A census of Î±-helical membrane proteins in double-stranded DNA viruses infecting bacteria and archaea. BMC Bioinformatics. 2015;16:380 pubmed publisher..The dramatic differences between the membrane proteomes of cells and viruses stem from the fact that viruses do not depend on essential membranes for energy transformation, ion homeostasis, nutrient transport and signaling. ..
- Koonin E, Wolf Y. Evolution of the CRISPR-Cas adaptive immunity systems in prokaryotes: models and observations on virus-host coevolution. Mol Biosyst. 2015;11:20-7 pubmed publisher..Such analyses are expected to yield disagreements with the predictions of the current, oversimplified models and to trigger a new round of theoretical developments. ..
- Koonin E. The meaning of biological information. Philos Trans A Math Phys Eng Sci. 2016;374: pubmed publisher..Thus, in order to adequately describe genome function and evolution, the concepts of information theory have to be adapted to incorporate the notion of meaning that is central to biology. ..
- Koonin E, Csuros M, Rogozin I. Whence genes in pieces: reconstruction of the exon-intron gene structures of the last eukaryotic common ancestor and other ancestral eukaryotes. Wiley Interdiscip Rev RNA. 2013;4:93-105 pubmed publisher..Alternative splicing most likely initially appeared as an inevitable result of splicing errors and only later was employed to generate structural and functional diversification of proteins. ..
- Mekhedov S, Makarova K, Koonin E. The complex domain architecture of SAMD9 family proteins, predicted STAND-like NTPases, suggests new links to inflammation and apoptosis. Biol Direct. 2017;12:13 pubmed publisher..These findings suggest that SAMD9 is a hub of a novel, evolutionarily conserved defense network that remains to be characterized. This article was reviewed by Igor B. Zhulin and Mensur Dlakic. ..
- Koonin E. Evolution of RNA- and DNA-guided antivirus defense systems in prokaryotes and eukaryotes: common ancestry vs convergence. Biol Direct. 2017;12:5 pubmed publisher..This article was reviewed by Mikhail Gelfand and Bojan Zagrovic. ..
- Makarova K, Wolf Y, Koonin E. Archaeal Clusters of Orthologous Genes (arCOGs): An Update and Application for Analysis of Shared Features between Thermococcales, Methanococcales, and Methanobacteriales. Life (Basel). 2015;5:818-40 pubmed publisher..The arCOGs are expected to be instrumental for a comprehensive phylogenomic study of the archaea. ..
- Koonin E, Dolja V, Krupovic M. Origins and evolution of viruses of eukaryotes: The ultimate modularity. Virology. 2015;479-480:2-25 pubmed publisher..Strikingly, evolution of all classes of eukaryotic viruses appears to have involved fusion between structural and replicative gene modules derived from different sources along with additional acquisitions of diverse genes. ..
- Koonin E, Novozhilov A. Origin and evolution of the genetic code: the universal enigma. IUBMB Life. 2009;61:99-111 pubmed publisher..A real understanding of the code origin and evolution is likely to be attainable only in conjunction with a credible scenario for the evolution of the coding principle itself and the translation system. ..
- Koonin E. Archaeal ancestors of eukaryotes: not so elusive any more. BMC Biol. 2015;13:84 pubmed publisher..The discovery of complex archaea that are the closest living relatives of eukaryotes is most compatible with the symbiogenetic scenario for eukaryogenesis. ..
- Faure G, Ogurtsov A, Shabalina S, Koonin E. Role of mRNA structure in the control of protein folding. Nucleic Acids Res. 2016;44:10898-10911 pubmed
- Koonin E, Aravind L. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ. 2002;9:394-404 pubmed
- Shmakov S, Abudayyeh O, Makarova K, Wolf Y, Gootenberg J, Semenova E, et al. Discovery and Functional Characterization of Diverse Class 2 CRISPR-Cas Systems. Mol Cell. 2015;60:385-97 pubmed publisher..Finally, comparative analysis indicates that Class 2 CRISPR-Cas systems evolved on multiple occasions through recombination of Class 1 adaptation modules with effector proteins acquired from distinct mobile elements. ..
- Puigbò P, Makarova K, Kristensen D, Wolf Y, Koonin E. Reconstruction of the evolution of microbial defense systems. BMC Evol Biol. 2017;17:94 pubmed publisher..Apart from the paucity and the low flux of defense genes in parasitic bacteria with deteriorating genomes, there is no clear connection between the evolutionary regime of defense systems and microbial life style. ..
- Koonin E, Krupovic M. Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity. Curr Opin Virol. 2017;25:7-15 pubmed publisher..Taken together, these findings show that Polintons, PLV, virophages and transpovirons form a dynamic network of integrating mobile genetic elements that contribute to the cellular antivirus defense and host-virus coevolution. ..
- ..Together with the unexpected discoveries of the first putative archaeal RNA virus and a RNA-DNA virus hybrid, this work shows that RNA viral genomics has major surprises to deliver. ..
- Koonin E, Wolf Y, PuigbÃ² P. The phylogenetic forest and the quest for the elusive tree of life. Cold Spring Harb Symp Quant Biol. 2009;74:205-13 pubmed publisher..The totality of gene trees comprising the FOL appears to be a natural representation of the history of life given the inherent tree-like character of the replication process. ..
- Makarova K, Ponomarev V, Koonin E. Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol. 2001;2:RESEARCH 0033 pubmed..The recurrent theme of emergence and disruption of Zn-ribbons in bacterial ribosomal proteins awaits a functional interpretation. ..
- Krupovic M, Koonin E. Self-synthesizing transposons: unexpected key players in the evolution of viruses and defense systems. Curr Opin Microbiol. 2016;31:25-33 pubmed publisher..The casposons are thought to have played a pivotal role in the origin of the prokaryotic adaptive immunity, giving rise to the adaptation module of the CRISPR-Cas systems. ..
- Koonin E, Wolf Y, Katsnelson M. Inevitability of the emergence and persistence of genetic parasites caused by evolutionary instability of parasite-free states. Biol Direct. 2017;12:31 pubmed publisher..This article has been reviewed by Yitzhak Pilpel, Bojan Zagrovic, and Eric van Nimwegen. ..
- Yutin N, Makarova K, Gussow A, Krupovic M, Segall A, Edwards R, et al. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat Microbiol. 2018;3:38-46 pubmed publisher..These findings provide for experimental characterization of the most abundant but poorly understood members of the human-associated virome. ..
- Krupovic M, Koonin E. Cellular origin of the viral capsid-like bacterial microcompartments. Biol Direct. 2017;12:25 pubmed publisher..This article was reviewed by Igor Zhulin, Jeremy Selengut and Narayanaswamy Srinivasan. For complete reviews, see the Reviewers' reports section. ..
- Shmakov S, Sitnik V, Makarova K, Wolf Y, SEVERINOV K, Koonin E. The CRISPR Spacer Space Is Dominated by Sequences from Species-Specific Mobilomes. MBio. 2017;8: pubmed publisher..We further demonstrate that spacers with no matches have the same properties as those of identifiable origins, strongly suggesting that all spacers originate from mobile elements. ..
- Koonin E, Makarova K. CRISPR-Cas: evolution of an RNA-based adaptive immunity system in prokaryotes. RNA Biol. 2013;10:679-86 pubmed publisher..Such coupling could manifest in the persistence state being induced and potentially providing conditions for more effective action of the immune system or in cell death being triggered when immunity fails. ..
- Lavysh D, Sokolova M, Minakhin L, Yakunina M, Artamonova T, Kozyavkin S, et al. The genome of AR9, a giant transducing Bacillus phage encoding two multisubunit RNA polymerases. Virology. 2016;495:185-96 pubmed publisher..Purification of one of PBS1/AR9 RNAPs has been reported previously, which makes AR9 a promising object for further studies of RNAP evolution, assembly and mechanism. ..
- Hudaiberdiev S, Shmakov S, Wolf Y, Terns M, Makarova K, Koonin E. Phylogenomics of Cas4 family nucleases. BMC Evol Biol. 2017;17:232 pubmed publisher..Experimental characterization of the solo and MGE-encoded Cas4 nucleases is expected to reveal currently uncharacterized defense and anti-defense systems and their interactions with CRISPR-Cas systems. ..
- Belinky F, Rogozin I, Koonin E. Selection on start codons in prokaryotes and potential compensatory nucleotide substitutions. Sci Rep. 2017;7:12422 pubmed publisher..Together, all these findings indicate that in prokaryotes, translation start signals are subject to weak but significant selection for maximization of initiation rate and, consequently, protein production...
- Koonin E, Wolf Y. Evolution of microbes and viruses: a paradigm shift in evolutionary biology?. Front Cell Infect Microbiol. 2012;2:119 pubmed
- Koonin E. Intron-dominated genomes of early ancestors of eukaryotes. J Hered. 2009;100:618-23 pubmed publisher..An organism with such an unusual genome architecture could survive only under conditions of a severe population bottleneck...
- Koonin E, Rudd K. Two domains of superfamily I helicases may exist as separate proteins. Protein Sci. 1996;5:178-80 pubmed..It is speculated that PhoH and YjhR have evolved from helicases through deletion of the portions of the helicase genes coding for the C- and N-terminal domain, respectively. ..
- Koonin E. Evolution of genome architecture. Int J Biochem Cell Biol. 2009;41:298-306 pubmed publisher..Selection for specific gene arrangements (elements of genome architecture) seems only to modulate the results of these processes. ..
- Koonin E, Makarova K, Elkins J. Orthologs of the small RPB8 subunit of the eukaryotic RNA polymerases are conserved in hyperthermophilic Crenarchaeota and "Korarchaeota". Biol Direct. 2007;2:38 pubmed..These findings suggest that all 12 core subunits of eukaryotic RNAPs were already present in the last common ancestor of the extant archaea...
- Koonin E. Viruses and mobile elements as drivers of evolutionary transitions. Philos Trans R Soc Lond B Biol Sci. 2016;371: pubmed publisher..This article is part of the themed issue 'The major synthetic evolutionary transitions'. ..