Home LiteratureArticle Details
PMID: 17708768 Published · epublish English Journal Article Research Support, N.I.H., Intramural

The Biological Big Bang model for the major transitions in evolution.

Biology direct ·Vol. 2 ·2007-08-20 ·Pages 21

Koonin EV

Abstract

Major transitions in biological evolution show the same pattern of sudden emergence of diverse forms at a new level of complexity. The relationships between major groups within an emergent new class of biological entities are hard to decipher and do not seem to fit the tree pattern that, following Darwin's original proposal, remains the dominant description of biological evolution. The cases in point include the origin of complex RNA molecules and protein folds; major groups of viruses; archaea and bacteria, and the principal lineages within each of these prokaryotic domains; eukaryotic supergroups; and animal phyla. In each of these pivotal nexuses in life's history, the principal "types" seem to appear rapidly and fully equipped with the signature features of the respective new level of biological organization. No intermediate "grades" or intermediate forms between different types are detectable. Usually, this pattern is attributed to cladogenesis compressed in time, combined with the inevitable erosion of the phylogenetic signal. I propose that most or all major evolutionary transitions that show the "explosive" pattern of emergence of new types of biological entities correspond to a boundary between two qualitatively distinct evolutionary phases. The first, inflationary phase is characterized by extremely rapid evolution driven by various processes of genetic information exchange, such as horizontal gene transfer, recombination, fusion, fission, and spread of mobile elements. These processes give rise to a vast diversity of forms from which the main classes of entities at the new level of complexity emerge independently, through a sampling process. In the second phase, evolution dramatically slows down, the respective process of genetic information exchange tapers off, and multiple lineages of the new type of entities emerge, each of them evolving in a tree-like fashion from that point on. This biphasic model of evolution incorporates the previously developed concepts of the emergence of protein folds by recombination of small structural units and origin of viruses and cells from a pre-cellular compartmentalized pool of recombining genetic elements. The model is extended to encompass other major transitions. It is proposed that bacterial and archaeal phyla emerged independently from two distinct populations of primordial cells that, originally, possessed leaky membranes, which made the cells prone to rampant gene exchange; and that the eukaryotic supergroups emerged through distinct, secondary endosymbiotic events (as opposed to the primary, mitochondrial endosymbiosis). This biphasic model of evolution is substantially analogous to the scenario of the origin of universes in the eternal inflation version of modern cosmology. Under this model, universes like ours emerge in the infinite multiverse when the eternal process of exponential expansion, known as inflation, ceases in a particular region as a result of false vacuum decay, a first order phase transition process. The result is the nucleation of a new universe, which is traditionally denoted Big Bang, although this scenario is radically different from the Big Bang of the traditional model of an expanding universe. Hence I denote the phase transitions at the end of each inflationary epoch in the history of life Biological Big Bangs (BBB). A Biological Big Bang (BBB) model is proposed for the major transitions in life's evolution. According to this model, each transition is a BBB such that new classes of biological entities emerge at the end of a rapid phase of evolution (inflation) that is characterized by extensive exchange of genetic information which takes distinct forms for different BBBs. The major types of new forms emerge independently, via a sampling process, from the pool of recombining entities of the preceding generation. This process is envisaged as being qualitatively different from tree-pattern cladogenesis.

MeSH Terms
Animals Biological Evolution Eukaryotic Cells Evolution, Molecular Gene Transfer, Horizontal Models, Biological Prokaryotic Cells Recombination, Genetic
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Koonin Eugene V
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. koonin@ncbi.nlm.nih.gov
References (96)
96 references, click to expand
  1. Bushes in the tree of life.
    PLoS Biol. 2006 Nov;4(11):e352 PMID: 17105342
  2. Lateral gene transfer and the nature of bacterial innovation.
    Nature. 2000 May 18;405(6784):299-304 PMID: 10830951
  3. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae.
    Mol Biol Evol. 2005 May;22(5):1299-308 PMID: 15746017
  4. Symbiosis as a mechanism of evolution: status of cell symbiosis theory.
    Symbiosis. 1985;1:101-24 PMID: 11543608
  5. Ancestral lipid biosynthesis and early membrane evolution.
    Trends Biochem Sci. 2004 Sep;29(9):469-77 PMID: 15337120
  6. Trends in protein evolution inferred from sequence and structure analysis.
    Curr Opin Struct Biol. 2002 Jun;12(3):392-9 PMID: 12127460
  7. Photosynthetic eukaryotes unite: endosymbiosis connects the dots.
    Bioessays. 2004 Jan;26(1):50-60 PMID: 14696040
  8. Evolutionary origins of genomic repertoires in bacteria.
    PLoS Biol. 2005 May;3(5):e130 PMID: 15799709
  9. The impact of comparative genomics on our understanding of evolution.
    Cell. 2000 Jun 9;101(6):573-6 PMID: 10892642
  10. The Cambrian "explosion" of metazoans and molecular biology: would Darwin be satisfied?
    Int J Dev Biol. 2003;47(7-8):505-15 PMID: 14756326
  11. The last eukaryotic common ancestor (LECA): acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon.
    Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):13080-5 PMID: 16938841
  12. Processivity of ribozyme-catalyzed RNA polymerization.
    Biochemistry. 2003 Jul 29;42(29):8748-55 PMID: 12873135
  13. Tracing the Thread of Plastid Diversity through the Tapestry of Life.
    Am Nat. 1999 Oct;154(S4):S164-S177 PMID: 10527925
  14. Speculations on the early course of evolution.
    Proc Natl Acad Sci U S A. 1986 Mar;83(5):1271-5 PMID: 2419905
  15. Tempo and mode in the macroevolutionary reconstruction of Darwinism.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6764-71 PMID: 8041695
  16. The hydrogen hypothesis for the first eukaryote.
    Nature. 1998 Mar 5;392(6671):37-41 PMID: 9510246
  17. Comparison of archaeal and bacterial genomes: computer analysis of protein sequences predicts novel functions and suggests a chimeric origin for the archaea.
    Mol Microbiol. 1997 Aug;25(4):619-37 PMID: 9379893
  18. Evolution of bacterial RNA polymerase: implications for large-scale bacterial phylogeny, domain accretion, and horizontal gene transfer.
    Gene. 2004 Jun 23;335:73-88 PMID: 15194191
  19. Is it time to uproot the tree of life?
    Science. 1999 May 21;284(5418):1305-7 PMID: 10383313
  20. Did DNA replication evolve twice independently?
    Nucleic Acids Res. 1999 Sep 1;27(17):3389-401 PMID: 10446225
  21. Inventing the dynamo machine: the evolution of the F-type and V-type ATPases.
    Nat Rev Microbiol. 2007 Nov;5(11):892-9 PMID: 17938630
  22. Genome trees and the nature of genome evolution.
    Annu Rev Microbiol. 2005;59:191-209 PMID: 16153168
  23. The evolution of eukaryotes.
    Science. 2007 Apr 27;316(5824):542-3; author reply 542-3 PMID: 17463271
  24. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates.
    Mol Biol Evol. 2007 Aug;24(8):1702-13 PMID: 17488740
  25. Automatic selection of representative proteins for bacterial phylogeny.
    BMC Evol Biol. 2005;5:34 PMID: 15927057
  26. The ancient Virus World and evolution of cells.
    Biol Direct. 2006 Sep 19;1:29 PMID: 16984643
  27. Holographic probabilities in eternal inflation.
    Phys Rev Lett. 2006 Nov 10;97(19):191302 PMID: 17155610
  28. Genome trees constructed using five different approaches suggest new major bacterial clades.
    BMC Evol Biol. 2001 Oct 20;1:8 PMID: 11734060
  29. On the evolution of protein folds: are similar motifs in different protein folds the result of convergence, insertion, or relics of an ancient peptide world?
    J Struct Biol. 2001 May-Jun;134(2-3):191-203 PMID: 11551179
  30. Gene regulatory networks and the evolution of animal body plans.
    Science. 2006 Feb 10;311(5762):796-800 PMID: 16469913
  31. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree.
    J Eukaryot Microbiol. 1999 Jul-Aug;46(4):347-66 PMID: 18092388
  32. Phylogenetic classification and the universal tree.
    Science. 1999 Jun 25;284(5423):2124-9 PMID: 10381871
  33. Introns and the origin of nucleus-cytosol compartmentalization.
    Nature. 2006 Mar 2;440(7080):41-5 PMID: 16511485
  34. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell.
    Nucleic Acids Res. 2005;33(14):4626-38 PMID: 16106042
  35. Expanding protein universe and its origin from the biological Big Bang.
    Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14132-6 PMID: 12384571
  36. Paradigm change in evolutionary microbiology.
    Stud Hist Philos Biol Biomed Sci. 2005 Mar;36(1):183-208 PMID: 16120264
  37. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences.
    Crit Rev Biochem Mol Biol. 1993;28(5):375-430 PMID: 8269709
  38. Molecular clocks do not support the Cambrian explosion.
    Mol Biol Evol. 2005 Mar;22(3):387-90 PMID: 15537810
  39. Common origin of four diverse families of large eukaryotic DNA viruses.
    J Virol. 2001 Dec;75(23):11720-34 PMID: 11689653
  40. A unifold, mesofold, and superfold model of protein fold use.
    Proteins. 2002 Jan 1;46(1):61-71 PMID: 11746703
  41. Genome trees and the tree of life.
    Trends Genet. 2002 Sep;18(9):472-9 PMID: 12175808
  42. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells.
    Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):59-83; discussion 83-5 PMID: 12594918
  43. The tree of eukaryotes.
    Trends Ecol Evol. 2005 Dec;20(12):670-6 PMID: 16701456
  44. Pattern pluralism and the Tree of Life hypothesis.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2043-9 PMID: 17261804
  45. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes.
    Trends Genet. 1998 Aug;14(8):307-11 PMID: 9724962
  46. The universal ancestor.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6854-9 PMID: 9618502
  47. Extreme accumulation of nucleotides in simulated hydrothermal pore systems.
    Proc Natl Acad Sci U S A. 2007 May 29;104(22):9346-51 PMID: 17494767
  48. The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate?
    Biol Direct. 2006 Aug 14;1:22 PMID: 16907971
  49. Eukaryotic evolution, changes and challenges.
    Nature. 2006 Mar 30;440(7084):623-30 PMID: 16572163
  50. Lateral genomics.
    Trends Cell Biol. 1999 Dec;9(12):M5-8 PMID: 10611671
  51. The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation.
    Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):1039-54 PMID: 16754613
  52. Estimating the number of protein folds.
    J Mol Biol. 1998 Dec 18;284(5):1301-5 PMID: 9878351
  53. The deep roots of eukaryotes.
    Science. 2003 Jun 13;300(5626):1703-6 PMID: 12805537
  54. Punctuated equilibrium comes of age.
    Nature. 1993 Nov 18;366(6452):223-7 PMID: 8232582
  55. Uprooting the tree of life.
    Sci Am. 2000 Feb;282(2):90-5 PMID: 10710791
  56. The new phylogeny of eukaryotes.
    Curr Opin Genet Dev. 2000 Dec;10(6):596-601 PMID: 11088007
  57. Genome-wide molecular clock and horizontal gene transfer in bacterial evolution.
    J Bacteriol. 2004 Oct;186(19):6575-85 PMID: 15375139
  58. An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences.
    BMC Evol Biol. 2005;5:36 PMID: 15932645
  59. Jumping genes and shrinking genomes--probing the evolution of eukaryotic photosynthesis with genomics.
    IUBMB Life. 2005 Aug;57(8):539-47 PMID: 16118111
  60. Fold change in evolution of protein structures.
    J Struct Biol. 2001 May-Jun;134(2-3):167-85 PMID: 11551177
  61. Assessment of phylogenomic and orthology approaches for phylogenetic inference.
    Bioinformatics. 2007 Apr 1;23(7):815-24 PMID: 17237036
  62. The string theory landscape.
    Sci Am. 2004 Sep;291(3):78-87 PMID: 15376755
  63. Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae).
    Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):109-33; discussion 133-4 PMID: 12594921
  64. An RNA-making reactor for the origin of life.
    Proc Natl Acad Sci U S A. 2007 May 29;104(22):9105-6 PMID: 17519331
  65. On the origin of genomes and cells within inorganic compartments.
    Trends Genet. 2005 Dec;21(12):647-54 PMID: 16223546
  66. Symbiont acquisition as neoseme: origin of species and higher taxa.
    Symbiosis. 1987;4:185-98 PMID: 11542098
  67. The cosmological model of eternal inflation and the transition from chance to biological evolution in the history of life.
    Biol Direct. 2007 May 31;2:15 PMID: 17540027
  68. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa.
    Int J Syst Evol Microbiol. 2002 Mar;52(Pt 2):297-354 PMID: 11931142
  69. Evaluating support for the current classification of eukaryotic diversity.
    PLoS Genet. 2006 Dec;2(12):e220 PMID: 17194223
  70. Archaea and the origin(s) of DNA replication proteins.
    Cell. 1997 Jun 27;89(7):995-8 PMID: 9215620
  71. Microbial mats and the early evolution of life.
    Trends Ecol Evol. 1990 May;5(5):140-4 PMID: 11538863
  72. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists.
    J Eukaryot Microbiol. 2005 Sep-Oct;52(5):399-451 PMID: 16248873
  73. Estimating the number of protein folds and families from complete genome data.
    J Mol Biol. 2000 Jun 16;299(4):897-905 PMID: 10843846
  74. Evolution. The Cambrian explosion exploded?
    Science. 2001 Jul 20;293(5529):438-9 PMID: 11463899
  75. Vertebrate genome evolution: a slow shuffle or a big bang?
    Bioessays. 1999 Aug;21(8):697-703 PMID: 10440866
  76. Genomics and the irreducible nature of eukaryote cells.
    Science. 2006 May 19;312(5776):1011-4 PMID: 16709776
  77. TreeView: an application to display phylogenetic trees on personal computers.
    Comput Appl Biosci. 1996 Aug;12(4):357-8 PMID: 8902363
  78. Cell evolution and Earth history: stasis and revolution.
    Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):969-1006 PMID: 16754610
  79. On punctuated equilibria.
    Science. 1997 Apr 18;276(5311):338-41 PMID: 9139351
  80. Diversity and evolutionary history of plastids and their hosts.
    Am J Bot. 2004 Oct;91(10):1481-93 PMID: 21652304
  81. Origin of bilaterian body plans: evolution of developmental regulatory mechanisms.
    Science. 1995 Nov 24;270(5240):1319-25 PMID: 7481819
  82. Evolution: red algal genome affirms a common origin of all plastids.
    Curr Biol. 2004 Jul 13;14(13):R514-6 PMID: 15242632
  83. Darwin's dilemma: the realities of the Cambrian 'explosion'.
    Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):1069-83 PMID: 16754615
  84. Evolution. A trigger for the Cambrian explosion?
    Science. 2002 Nov 22;298(5598):1547 PMID: 12446888
  85. Archaeal phylogeny based on proteins of the transcription and translation machineries: tackling the Methanopyrus kandleri paradox.
    Genome Biol. 2004;5(3):R17 PMID: 15003120
  86. Examining bacterial species under the specter of gene transfer and exchange.
    Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6595-9 PMID: 15851673
  87. Cosmology. Anthropic reasoning.
    Science. 2005 Aug 12;309(5737):1022-3 PMID: 16099967
  88. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima.
    Nature. 1999 May 27;399(6734):323-9 PMID: 10360571
  89. Horizontal gene transfer in prokaryotes: quantification and classification.
    Annu Rev Microbiol. 2001;55:709-42 PMID: 11544372
  90. Biogeochemistry of hypersaline microbial mats illustrates the dynamics of modern microbial ecosystems and the early evolution of the biosphere.
    Biol Bull. 2003 Apr;204(2):160-7 PMID: 12700147
  91. Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles.
    Trends Genet. 1998 Nov;14(11):442-4 PMID: 9825671
  92. On the evolution of cells.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8742-7 PMID: 12077305
  93. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses.
    Virus Res. 2006 Apr;117(1):156-84 PMID: 16494962
  94. Molecular dates for the "cambrian explosion": the influence of prior assumptions.
    Syst Biol. 2005 Aug;54(4):672-8 PMID: 16126662
  95. Animal evolution and the molecular signature of radiations compressed in time.
    Science. 2005 Dec 23;310(5756):1933-8 PMID: 16373569
  96. Inflationary cosmology: exploring the universe from the smallest to the largest scales.
    Science. 2005 Feb 11;307(5711):884-90 PMID: 15705842
Article Info
Journal
Biology direct
Abbr.
Biol Direct
ISSN
1745-6150
Published
2007-08-20
Epub
2007-00-20
Pages
21
Language
English
Region
England
NLM ID
101258412
PMCID
PMC1973067
Subset
IM
Grants
Intramural NIH HHS · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com