Systematic inference of highways of horizontal gene transfer in prokaryotes

MOTIVATION Horizontal gene transfer (HGT) plays a crucial role in the evolution of prokaryotic species. Typically, no more than a few genes are horizontally transferred between any two species. However, several studies identified pairs of species (or linages) between which many different genes were horizontally transferred. Such a pair is said to be linked by a highway of gene sharing. Inferring such highways is crucial to understanding the evolution of prokaryotes and for inferring past symbiotic and ecological associations among different species. RESULTS We present a new improved method for systematically detecting highways of gene sharing. As we demonstrate using a variety of simulated datasets, our method is highly accurate and efficient, and robust to noise and high rates of HGT. We further validate our method by applying it to a published dataset of >22 000 gene trees from 144 prokaryotic species. Our method makes it practical, for the first time, to perform accurate highway analysis quickly and easily even on large datasets with high rates of HGT. AVAILABILITY AND IMPLEMENTATION An implementation of the method can be freely downloaded from: http://acgt.cs.tau.ac.il/hide.

[1]  Ron Shamir,et al.  Detecting Highways of Horizontal Gene Transfer , 2010, RECOMB-CG.

[2]  W. Martin,et al.  The hydrogen hypothesis for the first eukaryote , 1998, Nature.

[3]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[4]  Michael Shmoish,et al.  Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. , 2005, Environmental microbiology.

[5]  C. V. Dohlen,et al.  Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts , 2001, Nature.

[6]  Tandy J. Warnow,et al.  Reconstructing reticulate evolution in species: theory and practice , 2004, RECOMB.

[7]  Satish Rao,et al.  Quartets MaxCut: A Divide and Conquer Quartets Algorithm , 2010, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[8]  Vladimir Makarenkov,et al.  New Efficient Algorithm for Detection of Horizontal Gene Transfer Events , 2003, WABI.

[9]  Burkhard Becker,et al.  Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes , 2008, BMC Evolutionary Biology.

[10]  Luay Nakhleh,et al.  Confounding Factors in HGT Detection: Statistical Error, Coalescent Effects, and Multiple Solutions , 2007, J. Comput. Biol..

[11]  Ali Tofigh,et al.  Using Trees to Capture Reticulate Evolution : Lateral Gene Transfers and Cancer Progression , 2009 .

[12]  Daniel H. Huson,et al.  Dendroscope: An interactive viewer for large phylogenetic trees , 2007, BMC Bioinformatics.

[13]  W. Doolittle,et al.  Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. , 2006, Genome research.

[14]  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.

[15]  Michael T. Hallett,et al.  Efficient algorithms for lateral gene transfer problems , 2001, RECOMB.

[16]  J. Peter Gogarten,et al.  Intertwined Evolutionary Histories of Marine Synechococcus and Prochlorococcus marinus , 2009, Genome biology and evolution.

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

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

[19]  Sagi Snir,et al.  Parsimony Score of Phylogenetic Networks: Hardness Results and a Linear-Time Heuristic , 2009, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[20]  K. Shimada,et al.  Horizontal Transfer of the Photosynthesis Gene Cluster and Operon Rearrangement in Purple Bacteria , 2001, Journal of Molecular Evolution.

[21]  Glenn Hickey,et al.  SPR Distance Computation for Unrooted Trees , 2008, Evolutionary bioinformatics online.

[22]  M. W. Gray,et al.  Origin and evolution of organelle genomes. , 1993, Current opinion in genetics & development.

[23]  Tanja Stadler,et al.  Sampling trees from evolutionary models. , 2010, Systematic biology.

[24]  Ahmed Moustafa,et al.  Chlamydiae Has Contributed at Least 55 Genes to Plantae with Predominantly Plastid Functions , 2008, PloS one.

[25]  V. Makarenkov,et al.  Inferring and validating horizontal gene transfer events using bipartition dissimilarity. , 2010, Systematic biology.

[26]  Michael T. Hallett,et al.  Simultaneous Identification of Duplications and Lateral Gene Transfers , 2011, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[27]  Vincent Berry,et al.  An Efficient Algorithm for Gene/Species Trees Parsimonious Reconciliation with Losses, Duplications and Transfers , 2010, RECOMB-CG.

[28]  Jörg Overmann,et al.  Phototrophic consortia: model systems for symbiotic interrelations between prokaryotes , 2002, Archives of Microbiology.

[29]  Charles Semple,et al.  On the Computational Complexity of the Rooted Subtree Prune and Regraft Distance , 2005 .

[30]  J R Roth,et al.  Selfish operons: horizontal transfer may drive the evolution of gene clusters. , 1996, Genetics.

[31]  Nicholas Hamilton,et al.  Phylogenetic identification of lateral genetic transfer events , 2006, BMC Evolutionary Biology.

[32]  Olga Zhaxybayeva,et al.  On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales , 2009, Proceedings of the National Academy of Sciences.

[33]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

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

[35]  Jinling Huang,et al.  Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? , 2007, Genome Biology.

[36]  Luay Nakhleh,et al.  RIATA-HGT: A Fast and Accurate Heuristic for Reconstructing Horizontal Gene Transfer , 2005, COCOON.

[37]  K. Strimmer,et al.  Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies , 1996 .

[38]  D. Dykhuizen,et al.  Recombination in Escherichia coli and the definition of biological species , 1991, Journal of bacteriology.

[39]  Manolo Gouy,et al.  Detecting lateral gene transfers by statistical reconciliation of phylogenetic forests , 2010, BMC Bioinformatics.

[40]  L. Wilkinson BACTERIA , 1952, The Lancet.

[41]  Robert Fredriksson,et al.  SPRIT: Identifying horizontal gene transfer in rooted phylogenetic trees , 2010, BMC Evolutionary Biology.

[42]  Leon Goldovsky,et al.  The net of life: reconstructing the microbial phylogenetic network. , 2005, Genome research.