A model of horizontal gene transfer and the bacterial phylogeny problem.

How much horizontal gene transfer (HGT) between species influences bacterial phylogenomics is a controversial issue. This debate, however, lacks any quantitative assessment of the impact of HGT on phylogenies and of the ability of tree-building methods to cope with such events. I introduce a Markov model of genome evolution with HGT, accounting for the constraints on time -- an HGT event can only occur between concomitantly living species. This model is used to simulate multigene sequence data sets with or without HGT. The consequences of HGT on phylogenomic inference are analyzed and compared to other well-known phylogenetic artefacts. It is found that supertree methods are quite robust to HGT, keeping high levels of performance even when gene trees are largely incongruent with each other. Gene tree incongruence per se is not indicative of HGT. HGT, however, removes the (otherwise observed) positive relationship between sequence length and gene tree congruence to the estimated species tree. Surprisingly, when applied to a bacterial and a eukaryotic multigene data set, this criterion rejects the HGT hypothesis for the former, but not the latter data set.

[1]  C. Woese,et al.  Phylogenetic structure of the prokaryotic domain: The primary kingdoms , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[2]  C. Woese,et al.  Bacterial evolution , 1987, Microbiological reviews.

[3]  M. Ragan.  Phylogenetic inference based on matrix representation of trees. , 1992, Molecular phylogenetics and evolution.

[4]  William R. Taylor,et al.  The rapid generation of mutation data matrices from protein sequences , 1992, Comput. Appl. Biosci..

[5]  M. Gouy,et al.  Molecular phylogeny of Eubacteria: a new multiple tree analysis method applied to 15 sequence data sets questions the monophyly of gram-positive bacteria. , 1994, Research in microbiology.

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

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

[8]  Bin Ma,et al.  From Gene Trees to Species Trees , 2000, SIAM J. Comput..

[9]  J. Huelsenbeck,et al.  A compound poisson process for relaxing the molecular clock. , 2000, Genetics.

[10]  N. Grishin,et al.  Genome trees constructed using five different approaches suggest new major bacterial clades , 2001, BMC Evolutionary Biology.

[11]  N. Galtier,et al.  Maximum-likelihood phylogenetic analysis under a covarion-like model. , 2001, Molecular biology and evolution.

[12]  Heather M. Amrine,et al.  Mitochondrial versus nuclear gene sequences in deep-level mammalian phylogeny reconstruction. , 2001, Molecular biology and evolution.

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

[14]  Hervé Philippe,et al.  Eubacterial phylogeny based on translational apparatus proteins. , 2002, Trends in genetics : TIG.

[15]  M. Gouy,et al.  A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history. , 2002, Genome research.

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

[17]  N. Moran,et al.  From Gene Trees to Organismal Phylogeny in Prokaryotes:The Case of the γ-Proteobacteria , 2003, PLoS biology.

[18]  Jeffrey D. Palmer,et al.  Widespread horizontal transfer of mitochondrial genes in flowering plants , 2003, Nature.

[19]  N. Moran,et al.  Phylogenetics and the Cohesion of Bacterial Genomes , 2003, Science.

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

[21]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[22]  Daniel Jameson,et al.  OGRe: a relational database for comparative analysis of mitochondrial genomes , 2003, Nucleic Acids Res..

[23]  M. Stanhope,et al.  Molecules consolidate the placental mammal tree. , 2004, Trends in ecology & evolution.

[24]  Eric Bapteste,et al.  Deduction of probable events of lateral gene transfer through comparison of phylogenetic trees by recursive consolidation and rearrangement , 2005, BMC Evolutionary Biology.

[25]  Andrew T. Lloyd,et al.  Evolution of the recA gene and the molecular phylogeny of bacteria , 1993, Journal of Molecular Evolution.

[26]  Guy Perrière,et al.  Horizontal Transfer of Two Operons Coding for Hydrogenases Between Bacteria and Archaea , 2005, Journal of Molecular Evolution.

[27]  Olga Zhaxybayeva,et al.  Genome mosaicism and organismal lineages. , 2004, Trends in genetics : TIG.

[28]  Yan Boucher,et al.  Phylogenetic reconstruction and lateral gene transfer. , 2004, Trends in microbiology.

[29]  H. Ochman,et al.  Quartet mapping and the extent of lateral transfer in bacterial genomes. , 2003, Molecular biology and evolution.

[30]  H. Philippe,et al.  Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. , 2005, Molecular biology and evolution.

[31]  Junhyong Kim,et al.  The Cobweb of Life Revealed by Genome-Scale Estimates of Horizontal Gene Transfer , 2005, PLoS biology.

[32]  N. Moran,et al.  Evolutionary Origins of Genomic Repertoires in Bacteria , 2005, PLoS biology.

[33]  Sylvain Gaillard,et al.  Bio++: a set of C++ libraries for sequence analysis, phylogenetics, molecular evolution and population genetics , 2006, BMC Bioinformatics.

[34]  M. Suchard.  Stochastic Models for Horizontal Gene Transfer , 2005, Genetics.

[35]  Timothy J. Harlow,et al.  Highways of gene sharing in prokaryotes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  W. Doolittle,et al.  Do orthologous gene phylogenies really support tree-thinking? , 2005, BMC Evolutionary Biology.

[37]  N. Galtier,et al.  Phylogeographic support for horizontal gene transfer involving sympatric bruchid species , 2006, Biology Direct.

[38]  W. Doolittle,et al.  Visualizing and assessing phylogenetic congruence of core gene sets: a case study of the gamma-proteobacteria. , 2006, Molecular biology and evolution.

[39]  Sagi Snir,et al.  Maximum likelihood of phylogenetic networks , 2006, Bioinform..

[40]  Radhey S. Gupta,et al.  The sequences of heat shock protein 40 (DnaJ) homologs provide evidence for a close evolutionary relationship between the Deinococcus- Thermus group and cyanobacteria , 1997, Journal of Molecular Evolution.