What tangled web: barriers to rampant horizontal gene transfer.

Dawkins in his The Selfish Gene(1) quite aptly applies the term "selfish" to parasitic repetitive DNA sequences endemic to eukaryotic genomes, especially vertebrates. Doolittle and Sapienza(2) as well as Orgel and Crick(3) enlivened this notion of selfish DNA with the identification of such repetitive sequences as remnants of mobile elements such as transposons. In addition, Orgel and Crick(3) associated parasitic DNA with a potential to outgrow their host genomes by propagating both vertically via conventional genome replication as well as infectiously by horizontal gene transfer (HGT) to other genomes. Still later, Doolittle(4) speculated that unchecked HGT between unrelated genomes so complicates phylogeny that the conventional representation of a tree of life would have to be replaced by a thicket or a web of life.(4) In contrast, considerable data now show that reconstructions based on whole genome sequences are consistent with the conventional "tree of life".(5-10) Here, we identify natural barriers that protect modern genome populations from the inroads of rampant HGT.

[1]  W. Doolittle,et al.  Prokaryotic evolution in light of gene transfer. , 2002, Molecular biology and evolution.

[2]  W. Hamilton.  The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[3]  B. Snel,et al.  Genome phylogeny based on gene content , 1999, Nature Genetics.

[4]  H. Ochman,et al.  Evolutionary dynamics of full genome content in Escherichia coli , 2000, The EMBO journal.

[5]  S. Nuzhdin.  Sure facts, speculations, and open questions about the evolution of transposable element copy number , 2004, Genetica.

[6]  Wolfgang Stephan,et al.  The evolutionary dynamics of repetitive DNA in eukaryotes , 1994, Nature.

[7]  W. Doolittle,et al.  Selfish genes, the phenotype paradigm and genome evolution , 1980, Nature.

[8]  C. Kurland,et al.  Reductive evolution of resident genomes. , 1998, Trends in microbiology.

[9]  H. Ochman,et al.  Molecular archaeology of the Escherichia coli genome. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  D. Neafsey,et al.  Genome size evolution in pufferfish: a comparative analysis of diodontid and tetraodontid pufferfish genomes. , 2003, Genome research.

[11]  D. Petrov,et al.  Evidence for DNA loss as a determinant of genome size. , 2000, Science.

[12]  C. Kurland,et al.  Evolution of microbial genomes: sequence acquisition and loss. , 2002, Molecular biology and evolution.

[13]  C. Kurland,et al.  Translational accuracy and the fitness of bacteria. , 1992, Annual review of genetics.

[14]  F. Crick,et al.  Selfish DNA: the ultimate parasite , 1980, Nature.

[15]  S. Fitz-Gibbon,et al.  Whole genome-based phylogenetic analysis of free-living microorganisms. , 1999, Nucleic acids research.

[16]  B. Levin,et al.  The biological cost of antibiotic resistance. , 1999, Current opinion in microbiology.

[17]  W. Hamilton.  The genetical evolution of social behaviour. II. , 1964, Journal of theoretical biology.

[18]  S. Brenner,et al.  Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome , 1993, Nature.

[19]  N. W. Davis,et al.  Genome sequence of enterohaemorrhagic Escherichia coli O157:H7 , 2001, Nature.

[20]  T. Gregory.  Genome size and developmental complexity , 2002, Genetica.

[21]  B. Snel,et al.  SHOT: a web server for the construction of genome phylogenies. , 2002, Trends in genetics : TIG.

[22]  C. Woese.  The universal ancestor. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  U. Varshney,et al.  Specific interaction between the ribosome recycling factor and the elongation factor G from Mycobacterium tuberculosis mediates peptidyl‐tRNA release and ribosome recycling in Escherichia coli , 2001, The EMBO journal.

[24]  C. Kurland.  Something for everyone , 2000, EMBO reports.

[25]  H. Ochman,et al.  Amelioration of Bacterial Genomes: Rates of Change and Exchange , 1997, Journal of Molecular Evolution.

[26]  L. Orgel,et al.  Phylogenetic Classification and the Universal Tree , 1999 .

[27]  M. Matzke,et al.  Host defenses to parasitic sequences and the evolution of epigenetic control mechanisms , 2004, Genetica.

[28]  B. Dujon,et al.  The genomic tree as revealed from whole proteome comparisons. , 1999, Genome research.

[29]  Carl T. Bergstrom,et al.  Natural selection, infectious transfer and the existence conditions for bacterial plasmids. , 2000, Genetics.

[30]  C. Kurland,et al.  Horizontal gene transfer: A critical view , 2003 .

[31]  S. Mann,et al.  Paradigm lost , 1993, Nature.

[32]  P. McSweeney.  Something for everyone. , 1988, Nursing times.

[33]  M. M. Green.  Transposable elements in Drosophila and other Diptera. , 1980, Annual review of genetics.

[34]  H. Ishikawa.  Insect Symbiosis: An Introduction , 2003 .

[35]  Doolittle Wf.  Phylogenetic Classification and the Universal Tree , 1999 .

[36]  D. Petrov,et al.  High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. , 1998, Molecular biology and evolution.

[37]  B. Charlesworth,et al.  The population genetics of Drosophila transposable elements. , 1989, Annual review of genetics.

[38]  C. Woese.  Interpreting the universal phylogenetic tree. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[39]  O. Berg,et al.  Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. , 2000, Science.

[40]  C. Squires,et al.  An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[41]  N. Moran,et al.  Deletional bias and the evolution of bacterial genomes. , 2001, Trends in genetics : TIG.

[42]  R. Lewontin.  ‘The Selfish Gene’ , 1977, Nature.

[43]  Michael J. Stanhope,et al.  Universal trees based on large combined protein sequence data sets , 2001, Nature Genetics.

[44]  C. Kurland,et al.  The global phylogeny of glycolytic enzymes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[45]  S. Hooper,et al.  Gene Import or Deletion: A Study of the Different Genes in Escherichia coli Strains K12 and O157:H7 , 2002, Journal of Molecular Evolution.

[46]  Wen-Hsiung Li,et al.  Allelic Variation in the Squirrel Monkey X-Linked Color Vision Gene: Biogeographical and Behavioral Correlates , 2002, Journal of Molecular Evolution.

[47]  D. Hartl.  Molecular melodies in high and low C , 2000, Nature Reviews Genetics.

[48]  Tetsuya Hayashi,et al.  Molecular Cloning, Sequencing, Purification, and Characterization of Pseudomonas aeruginosa Ribosome Recycling Factor , 1999, Journal of bacteriology.

[49]  B. Snel,et al.  Genomes in flux: the evolution of archaeal and proteobacterial gene content. , 2002, Genome research.

[50]  F. Taddei,et al.  Role of mutator alleles in adaptive evolution , 1997, Nature.

[51]  T. Gregory,et al.  Insertion-deletion biases and the evolution of genome size. , 2004, Gene.