Evolutionary implications of horizontal gene transfer.

The flow of genes between different species represents a form of genetic variation whose implications have not been fully appreciated. Here I examine some key findings on the extent of horizontal gene transfer (HGT) revealed by comparative genome analysis and their theoretical implications. In theoretical terms, HGT affects ideas pertaining to the tree of life, the notion of a last universal common ancestor, and the biological unities, as well as the rules of taxonomic nomenclature. This review discusses the emergence of the eukaryotic cell and the occurrence of HGT among metazoan phyla involving both transposable elements and structural genes for normal housekeeping functions. I also discuss the bacterial pangenome, which provides an important case study on the permeability of species boundaries. An interesting observation about bdelloid rotifers and their reversion to asexual reproduction as it pertains to HGT is included.

[1]  D. Huson,et al.  A Survey of Combinatorial Methods for Phylogenetic Networks , 2010, Genome biology and evolution.

[2]  L. Hurst,et al.  The Genetic Code Is One in a Million , 1998, Journal of Molecular Evolution.

[3]  E. Danchin,et al.  Horizontal gene transfer in nematodes: a catalyst for plant parasitism? , 2011, Molecular plant-microbe interactions : MPMI.

[4]  N. Buisine,et al.  The Human SETMAR Protein Preserves Most of the Activities of the Ancestral Hsmar1 Transposase , 2006, Molecular and Cellular Biology.

[5]  C. Feschotte,et al.  Rampant horizontal transfer of SPIN transposons in squamate reptiles. , 2012, Molecular biology and evolution.

[6]  M. Hurles,et al.  Evidence for widespread reticulate evolution within human duplicons. , 2005, American journal of human genetics.

[7]  Bernard Henrissat,et al.  Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes , 2010, Proceedings of the National Academy of Sciences.

[8]  M. Ilan,et al.  Diversity of sponge mitochondrial introns revealed by cox 1 sequences of Tetillidae , 2010, BMC Evolutionary Biology.

[9]  M. Meselson,et al.  Massive Horizontal Gene Transfer in Bdelloid Rotifers , 2008, Science.

[10]  M. Huynen,et al.  Mosaic origin of the mitochondrial proteome , 2010, Proteomics.

[11]  M. Syvanen,et al.  Cross-species gene transfer; implications for a new theory of evolution. , 1985, Journal of theoretical biology.

[12]  Nobuyoshi Nakajima,et al.  Seeds of a Possible Natural Hybrid between Herbicide-Resistant Brassica napus and Brassica rapa Detected on a Riverbank in Japan , 2011, GM crops.

[13]  Loren H Rieseberg,et al.  A genomic view of introgression and hybrid speciation. , 2007, Current opinion in genetics & development.

[14]  Michael S. Barker,et al.  Comparative Genomic and Population Genetic Analyses Indicate Highly Porous Genomes and High Levels of Gene Flow between Divergent Helianthus Species , 2009, Evolution; international journal of organic evolution.

[15]  M. Groenen,et al.  Widespread horizontal genomic exchange does not erode species barriers among sympatric ducks , 2012, BMC Evolutionary Biology.

[16]  Davide Pisani,et al.  Supertrees disentangle the chimerical origin of eukaryotic genomes. , 2007, Molecular biology and evolution.

[17]  M. Morange Some considerations on the nature of LUCA, and the nature of life. , 2011, Research in microbiology.

[18]  M. Syvanen,et al.  WHOLE GENOME COMPARISONS REVEALS A POSSIBLE CHIMERIC ORIGIN FOR A MAJOR METAZOAN ASSEMBLAGE , 2010 .

[19]  J. L. Argueso,et al.  Mismatch repair proteins: key regulators of genetic recombination , 2004, Cytogenetic and Genome Research.

[20]  Bernard Labedan,et al.  The Last Universal Common Ancestor: emergence, constitution and genetic legacy of an elusive forerunner , 2008, Biology Direct.

[21]  M. G. Kidwell Lateral transfer in natural populations of eukaryotes. , 1993, Annual review of genetics.

[22]  M. Syvanen The evolutionary implications of mobile genetic elements. , 1984, Annual review of genetics.

[23]  R. Hromas,et al.  The transposase domain protein Metnase/SETMAR suppresses chromosomal translocations. , 2010, Cancer genetics and cytogenetics.

[24]  Natalia N Pouchkina-Stantcheva,et al.  Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae , 2011, Journal of Experimental Biology.

[25]  Jaideep P. Sundaram,et al.  Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  François Taddei,et al.  Evolutionary Implications of the Frequent Horizontal Transfer of Mismatch Repair Genes , 2000, Cell.

[27]  R. W. Davis,et al.  Functional genetic expression of eukaryotic DNA in Escherichia coli. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[28]  P. Long,et al.  Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis, have microbial origins , 2008, Proceedings of the National Academy of Sciences.

[29]  N. Goldenfeld,et al.  Collective evolution and the genetic code. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Wen-Hsiung Li,et al.  Dating the age of the last common ancestor of all living organisms with a protein clock , 2002 .

[31]  Cédric Feschotte,et al.  Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. , 2010, Trends in ecology & evolution.

[32]  Ralph Bock,et al.  Horizontal transfer of chloroplast genomes between plant species , 2012, Proceedings of the National Academy of Sciences.

[33]  C. Feschotte,et al.  A role for host–parasite interactions in the horizontal transfer of transposons across phyla , 2010, Nature.

[34]  P. Sharp,et al.  Determinants of DNA sequence divergence betweenEscherichia coli andSalmonella typhimurium: Codon usage, map position, and concerted evolution , 1991, Journal of Molecular Evolution.

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

[36]  A. Mathieu,et al.  Suppression of homologous and homeologous recombination by the bacterial MutS2 protein. , 2005, Molecular cell.

[37]  P. Servant,et al.  Mismatch repair ensures fidelity of replication and recombination in the radioresistant organism Deinococcus radiodurans , 2004, Molecular Genetics and Genomics.

[38]  Eugene V Koonin,et al.  The common ancestry of life , 2010, Biology Direct.

[39]  M. Radman,et al.  Mechanism and control of interspecies recombination in Escherichia coli. I. Mismatch repair, methylation, recombination and replication functions. , 1998, Genetics.

[40]  C. David,et al.  A genomic view of 500 million years of cnidarian evolution. , 2011, Trends in genetics : TIG.

[41]  P. Roberts,et al.  Plant parasitic nematodes: digesting a page from the microbe book. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Syvanen,et al.  On the Occurrence of Horizontal Gene Transfer Among an Arbitrarily Chosen Group of 26 Genes , 2002, Journal of Molecular Evolution.

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

[44]  H. Muller THE RELATION OF RECOMBINATION TO MUTATIONAL ADVANCE. , 1964, Mutation research.

[45]  Simon H. Martin,et al.  Butterfly genome reveals promiscuous exchange of mimicry adaptations among species , 2012, Nature.

[46]  A. Mushegian Gene content of LUCA, the last universal common ancestor. , 2008, Frontiers in bioscience : a journal and virtual library.

[47]  N. Satoh,et al.  The evolutionary origin of animal cellulose synthase , 2004, Development Genes and Evolution.

[48]  Simone Linz,et al.  Quantifying Hybridization in Realistic Time , 2011, J. Comput. Biol..

[49]  L. Koski,et al.  Codon bias and base composition are poor indicators of horizontally transferred genes. , 2001, Molecular biology and evolution.

[50]  F. Taddei,et al.  Costs and Benefits of High Mutation Rates: Adaptive Evolution of Bacteria in the Mouse Gut , 2001, Science.

[51]  H. Matsuda,et al.  Biased biological functions of horizontally transferred genes in prokaryotic genomes , 2004, Nature Genetics.

[52]  M. Steel,et al.  A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. , 2004, Molecular biology and evolution.

[53]  Anna G. Green,et al.  A Rooted Net of Life , 2011, Biology Direct.

[54]  L. Excoffier,et al.  Strong reproductive isolation between humans and Neanderthals inferred from observed patterns of introgression , 2011, Proceedings of the National Academy of Sciences.

[55]  D. Theobald On universal common ancestry, sequence similarity, and phylogenetic structure: the sins of P-values and the virtues of Bayesian evidence , 2011, Biology Direct.

[56]  Hyman Hartman,et al.  The origin of the eukaryotic cell: A genomic investigation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[57]  H. Ochman,et al.  Bacterial genomes as new gene homes: the genealogy of ORFans in E. coli. , 2004, Genome research.

[58]  F. Lapointe,et al.  Hybrids and Phylogenetics Revisited: A Statistical Test of Hybridization Using Quartets , 2007 .

[59]  M. Syvanen Recent emergence of the modern genetic code: a proposal. , 2002, Trends in genetics : TIG.

[60]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[61]  K. Moriguchi,et al.  Screening for yeast mutants defective in recipient ability for transkingdom conjugation with Escherichia coli revealed importance of vacuolar ATPase activity in the horizontal DNA transfer phenomenon. , 2012, Microbiological research.

[62]  S. Kanaya,et al.  Origin of eukaryotic cell nuclei by symbiosis of Archaea in Bacteria is revealed by homology-hit analysis , 2001, Nature Cell Biology.

[63]  J. Reitner,et al.  A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy , 2011, BMC Evolutionary Biology.

[64]  J. Krajčovič,et al.  The falsifiability of the models for the origin of eukaryotes , 2011, Current Genetics.

[65]  S. Richards,et al.  Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes , 2007, Science.

[66]  N. Whiteman,et al.  Parasitology: Nematode debt to bacteria , 2010, Nature.

[67]  N. Gerardo,et al.  Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae , 2012, Biology Letters.

[68]  Bradd J. Haley,et al.  Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae , 2009, Proceedings of the National Academy of Sciences.

[69]  Benjamin M. Wheeler,et al.  The dynamic genome of Hydra , 2010, Nature.

[70]  J. Peter Gogarten,et al.  Molecular Evolution of Aminoacyl tRNA Synthetase Proteins in the Early History of Life , 2011, Origins of Life and Evolution of Biospheres.

[71]  Marie-Agnès Petit,et al.  The λ Red Proteins Promote Efficient Recombination between Diverged Sequences: Implications for Bacteriophage Genome Mosaicism , 2008, PLoS genetics.

[72]  E. Bapteste,et al.  Horizontal gene transfer and the evolution of cnidarian stinging cells , 2008, Current Biology.

[73]  Michael Y. Galperin,et al.  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 , 2003, BMC Evolutionary Biology.

[74]  J. McInerney,et al.  Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function , 2010, Proceedings of the National Academy of Sciences.

[75]  J. Doyle,et al.  Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee , 2012, Proceedings of the National Academy of Sciences.

[76]  Ruben E. Valas,et al.  Structural analysis of polarizing indels : an emerging consensus on the root of the tree of life , 2009 .

[77]  J. Palmer,et al.  Horizontal gene transfer in eukaryotic evolution , 2008, Nature Reviews Genetics.

[78]  F. Taddei,et al.  Interspecies Recombination and Mismatch Repair , 2000 .

[79]  R. Hromas,et al.  Metnase/SETMAR: a domesticated primate transposase that enhances DNA repair, replication, and decatenation , 2010, Genetica.

[80]  J A Eisen,et al.  A phylogenomic study of the MutS family of proteins. , 1998, Nucleic acids research.

[81]  T. Vogel,et al.  Horizontal Gene Transfer Regulation in Bacteria as a “Spandrel” of DNA Repair Mechanisms , 2007, PloS one.

[82]  Motomi Ito,et al.  Reticulate evolution in the Crepidomanes minutum species complex (Hymenophyllaceae). , 2011, American journal of botany.

[83]  D. W. Kim,et al.  Genomic evolution of Vibrio cholerae. , 2010, Current opinion in microbiology.

[84]  Marlen S. Clark,et al.  Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods , 2008, Proceedings of the National Academy of Sciences.

[85]  W. Doolittle,et al.  The practice of classification and the theory of evolution, and what the demise of Charles Darwin's tree of life hypothesis means for both of them , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[86]  Douglas L. Theobald,et al.  A formal test of the theory of universal common ancestry , 2010, Nature.

[87]  Laurence D. Hurst,et al.  A quantitative measure of error minimization in the genetic code , 1991, Journal of Molecular Evolution.

[88]  P. Davies,et al.  Lateral Transfer of a Lectin-Like Antifreeze Protein Gene in Fishes , 2008, PloS one.

[89]  B. Henrissat,et al.  Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[91]  J. Lake Evidence for an early prokaryotic endosymbiosis , 2009, Nature.

[92]  R. Doolittle,et al.  Determining Divergence Times of the Major Kingdoms of Living Organisms with a Protein Clock , 1996, Science.

[93]  N. Moran,et al.  Lateral Transfer of Genes from Fungi Underlies Carotenoid Production in Aphids , 2010, Science.

[94]  D. Devos,et al.  Transitional forms between the three domains of life and evolutionary implications , 2011, Proceedings of the Royal Society B: Biological Sciences.

[95]  M. Hasegawa,et al.  Was the universal common ancestry proved? , 2010, Nature.

[96]  P. Gajer,et al.  The Pangenome Structure of Escherichia coli: Comparative Genomic Analysis of E. coli Commensal and Pathogenic Isolates , 2008, Journal of bacteriology.

[97]  H. Hartman,et al.  The origin of the eukaryotic cell. , 1984, Speculations in science and technology.

[98]  W. Martin,et al.  The tree of one percent , 2006, Genome Biology.

[99]  J. Lake,et al.  Horizontal gene transfer among genomes: the complexity hypothesis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[100]  R. Sommer,et al.  Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover , 2011, BMC Evolutionary Biology.

[101]  M. Batzer,et al.  Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[102]  Christoph Grunau,et al.  No evidence for lateral gene transfer between salmonids and schistosomes , 2010, Nature Genetics.

[103]  M. Syvanen Horizontal gene transfer: evidence and possible consequences. , 1994, Annual review of genetics.

[104]  James J. Davis,et al.  Similarity of genes horizontally acquired by Escherichia coli and Salmonella enterica is evidence of a supraspecies pangenome , 2011, Proceedings of the National Academy of Sciences.

[105]  E. Koonin,et al.  Search for a 'Tree of Life' in the thicket of the phylogenetic forest , 2009, Journal of biology.