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Detecting Laterally Transferred Genes

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Evolutionary Genomics

Part of the book series: Methods in Molecular Biology ((MIMB,volume 855))

Abstract

Methods for identifying alien genes in genomes fall into two general classes. Phylogenetic methods examine the distribution of a gene’s homologues among genomes to find those with relationships not consistent with vertical inheritance. These approaches include identifying orphan genes which lack homologues in closely related genomes and genes with unduly high levels of similarity to genes in otherwise unrelated genomes. Rigorous statistical tests are available to place confidence intervals for predicted alien genes. Parametric methods examine the compositional properties of genes within a genome to find those with atypical properties, likely indicating the directional mutational pressures of a donor genome. These methods may compare the properties of genes to genomic averages, properties of genes to each other, or properties of large, multigene regions of the chromosome. Here, we discuss the strengths and weaknesses of each approach.

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References

  1. Mayr, E (1942) Systematics and the Origin of Species, Columbia University Press, New York.

    Google Scholar 

  2. Lederberg, J, and Tatum, EL. (1946) Gene recombination in Escherichia coli. Nature 158, 558.

    CAS  Google Scholar 

  3. Ochia, K, Yamanaka, K, Kimura, K, et al. (1959) Inheritance of drug resistance (and its transfer) between Shigella strains and between Shigella and E. coli strains. Nihon Iji Shimpo 1861, 34.

    Google Scholar 

  4. Zinder, ND, and Lederberg, J. (1952) Genetic exchange in Salmonella. J. Bacteriol. 64, 679–697.

    PubMed  CAS  Google Scholar 

  5. Avery, OT, MacLeod, CM, and McCarty, M. (1944) Studies on the chemical nature of the substance inducing transformation of Pneumococcal types. J. Exper. Med. 79, 137–158.

    Article  CAS  Google Scholar 

  6. Doolittle, WF. (1999) Phylogenetic classification and the universal tree. Science 284, 2124–2129.

    Article  PubMed  CAS  Google Scholar 

  7. Ochman, H, Lawrence, JG, and Groisman, E. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304.

    Article  PubMed  CAS  Google Scholar 

  8. Welch, RA, Burland, V, Plunkett, G, 3rd, et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci., USA 99, 17020–17024.

    Article  CAS  Google Scholar 

  9. Hao, W, and Golding, GB. (2004) Patterns of bacterial gene movement. Mol Biol Evol 21, 1294–1307.

    Article  PubMed  CAS  Google Scholar 

  10. Hao, W, and Golding, GB. (2006) The fate of laterally transferred genes: life in the fast lane to adaptation or death. Genome Res 16, 636–643.

    Article  PubMed  CAS  Google Scholar 

  11. Dobrindt, U, Hochhut, B, Hentschel, U, et al. (2004) Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2, 414–424.

    Article  PubMed  CAS  Google Scholar 

  12. Hacker, J, Blum-Oehler, G, Muhldorfer, I, et al. (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol. Microbiol. 23, 1089–1097.

    Article  PubMed  CAS  Google Scholar 

  13. Hacker, J, and Kaper, JB. (2000) Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54, 641–679.

    Article  PubMed  CAS  Google Scholar 

  14. Zuckerkandl, E, and Pauling, L. (1965) Molecules as documents of evolutionary history. J. Theoret. Biol. 8, 357–366.

    Article  CAS  Google Scholar 

  15. Bapteste, E, Boucher, Y, Leigh, J, et al. (2004) Phylogenetic reconstruction and lateral gene transfer. Trends Microbiol 12, 406–411.

    Article  PubMed  CAS  Google Scholar 

  16. Bapteste, E, O’Malley, MA, Beiko, RG, et al. (2009) Prokaryotic evolution and the tree of life are two different things. Biol Direct 4, 34.

    Article  PubMed  Google Scholar 

  17. Gogarten, JP, Doolittle, WF, and Lawrence, JG. (2002) Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19, 2226–2238.

    Article  PubMed  CAS  Google Scholar 

  18. Koonin, EV, and Wolf, YI. (2009) The fundamental units, processes and patterns of evolution, and the tree of life conundrum. Biol Direct 4, 33.

    Article  PubMed  Google Scholar 

  19. Beiko, RG, Harlow, TJ, and Ragan, MA. (2005) Highways of gene sharing in prokaryotes. Proc. Natl. Acad. Sci., USA 102, 14332–14337.

    Article  CAS  Google Scholar 

  20. Poptsova, MS, and Gogarten, JP. (2007) BranchClust: a phylogenetic algorithm for selecting gene families. BMC Bioinformatics 8, 120.

    Article  PubMed  Google Scholar 

  21. Altenhoff, AM, Schneider, A, Gonnet, GH, et al. (2011) OMA 2011: orthology inference among 1000 complete genomes. Nucleic Acids Res 39, D289–294.

    Article  PubMed  Google Scholar 

  22. Koonin, EV. (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39, 309–338.

    Article  PubMed  CAS  Google Scholar 

  23. Clarke, GD, Beiko, RG, Ragan, MA, et al. (2002) Inferring genome trees by using a filter to eliminate phylogenetically discordant sequences and a distance matrix based on mean normalized BLASTP scores. J. Bacteriol. 184, 2072–2080.

    Article  PubMed  CAS  Google Scholar 

  24. MacLeod, D, Charlebois, RL, Doolittle, F, et al. (2005) Deduction of probable events of lateral gene transfer through comparison of phylogenetic trees by recursive consolidation and rearrangement. BMC Evol. Biol. 5, 27.

    Article  PubMed  Google Scholar 

  25. Zhaxybayeva, O, Gogarten, JP, Charlebois, RL, et al. (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16, 1099–1108.

    Article  PubMed  CAS  Google Scholar 

  26. Garcia-Vallve, S, Romeu, A, and Palau, J. (2000) Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol. Biol. Evol. 17, 352–361.

    Article  PubMed  CAS  Google Scholar 

  27. International Human Genome Sequencing Consortium. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860–921.

    Article  Google Scholar 

  28. Salzberg, SL, White, O, Peterson, J, et al. (2001) Microbial genes in the human genome: lateral transfer or gene loss? Science 292, 1903–1906.

    Article  PubMed  CAS  Google Scholar 

  29. Lawrence, JG, and Hartl, DL. (1992) Inference of horizontal genetic transfer: An approach using the bootstrap. Genetics 131, 753–760.

    PubMed  CAS  Google Scholar 

  30. Dessimoz, C, Margadant, D, and Gonnet, GH. (2008) DLIGHT – Lateral gene transfer detection using pairwise evolutionary distances in a statistical framework. RECOMB 2008, 315–330.

    Google Scholar 

  31. Raymond, J, Zhaxybayeva, O, Gogarten, JP, et al. (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298, 1616–1620.

    Article  PubMed  CAS  Google Scholar 

  32. Retchless, AC, and Lawrence, JG. (2010) Phylogenetic incongruence arising from fragmented speciation in enteric bacteria. Proc. Natl. Acad. Sci., USA 107, 11453–11458.

    Article  CAS  Google Scholar 

  33. Chan, CX, Darling, AE, Beiko, RG, et al. (2009) Are protein domains modules of lateral genetic transfer? PLoS One 4, e4524.

    Article  PubMed  Google Scholar 

  34. Chan, CX, Beiko, RG, Darling, AE, et al. (2009) Lateral transfer of genes and gene fragments in prokaryotes. Genome Biol Evol 1, 429–438.

    Article  PubMed  Google Scholar 

  35. Inagaki, Y, Susko, E, and Roger, AJ. (2006) Recombination between elongation factor 1alpha genes from distantly related archaeal lineages. Proc Natl Acad Sci U S A 103, 4528–4533.

    Article  PubMed  CAS  Google Scholar 

  36. Omelchenko, MV, Makarova, KS, Wolf, YI, et al. (2003) Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol 4, R55.

    Article  PubMed  Google Scholar 

  37. Makarenkov, V, Boc, A, Xie, J, et al. (2010) Weighted bootstrapping: a correction method for assessing the robustness of phylogenetic trees. BMC Evol Biol 10, 250.

    Article  PubMed  Google Scholar 

  38. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.

    Article  Google Scholar 

  39. Shimodaira, H, and Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16, 1114–1116.

    Article  CAS  Google Scholar 

  40. Shimodaira, H. (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51, 492–508.

    Article  PubMed  Google Scholar 

  41. Poptsova, MS, and Gogarten, JP. (2007) The power of phylogenetic approaches to detect horizontally transferred genes. BMC Evol Biol 7, 45.

    Article  PubMed  Google Scholar 

  42. Boc, A, Philippe, H, and Makarenkov, V. (2010) Inferring and validating horizontal gene transfer events using bipartition dissimilarity. Syst Biol 59, 195–211.

    Article  PubMed  CAS  Google Scholar 

  43. Lento, GM, Hickson, RE, Chambers, GK, et al. (1995) Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol Biol Evol 12, 28–52.

    Article  PubMed  CAS  Google Scholar 

  44. Zhaxybayeva, O, Lapierre, P, and Gogarten, JP. (2004) Genome mosaicism and organismal lineages. Trends Genet 20, 254–260.

    Article  PubMed  CAS  Google Scholar 

  45. Beiko, RG, and Ragan, MA. (2008) Detecting lateral genetic transfer: a phylogenetic approach. Methods Mol. Biol. 452, 457–469.

    Article  PubMed  CAS  Google Scholar 

  46. Beiko, RG, and Hamilton, N. (2006) Phylogenetic identification of lateral genetic transfer events. BMC Evol. Biol. 6, 15.

    Article  PubMed  Google Scholar 

  47. Beiko, RG, and Ragan, MA. (2009) Untangling hybrid phylogenetic signals: horizontal gene transfer and artifacts of phylogenetic reconstruction. Methods Mol Biol 532, 241–256.

    Article  PubMed  CAS  Google Scholar 

  48. Winfield, MD, and Groisman, EA. (2004) Phenotypic differences between Salmonella and Escherichia coli resulting from the disparate regulation of homologous genes. Proc. Natl. Acad. Sci., USA 101, 17162–17167.

    Article  CAS  Google Scholar 

  49. Daubin, V, and Ochman, H. (2004) Quartet mapping and the extent of lateral transfer in bacterial genomes. Mol. Biol. Evol. 21, 86–89.

    Article  PubMed  CAS  Google Scholar 

  50. Daubin, V, Moran, NA, and Ochman, H. (2003) Phylogenetics and the cohesion of bacterial genomes. Science 301, 829–832.

    Article  PubMed  CAS  Google Scholar 

  51. Bapteste, E, Susko, E, Leigh, J, et al. (2005) Do orthologous gene phylogenies really support tree-thinking? BMC Evol. Biol. 5, 33.

    CAS  Google Scholar 

  52. Ochman, H, and Lawrence, JG. (1996) Phylogenetics and the amelioration of bacterial genomes, in Escherichia coli and Salmonella typhimurium: Cellular and molecular biology, 2nd edition (Neidhardt, FC, Curtiss III, R, Ingraham, JL, et al., Eds.), pp 2627–2637, American Society for Microbiology, Washington, D.C.

    Google Scholar 

  53. Lawrence, JG, and Ochman, H. (1997) Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol. 44, 383–397.

    Article  PubMed  CAS  Google Scholar 

  54. Lawrence, JG, and Ochman, H. (1998) Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci., USA 95, 9413–9417.

    Article  CAS  Google Scholar 

  55. Karlin, S, and Burge, C. (1995) Dinucleotide relative abundance extremes: a genomic signature. Trends Genet. 11, 283–290.

    Article  PubMed  CAS  Google Scholar 

  56. Karlin, S. (1998) Global dinucleotide signatures and analysis of genomic heterogeneity. Curr. Opin. Microbiol. 1, 598–610.

    Article  PubMed  CAS  Google Scholar 

  57. Hooper, SD, and Berg, OG. (2002) Detection of genes with atypical nucleotide sequence in microbial genomes. J. Mol. Evol. 54, 365–375.

    PubMed  CAS  Google Scholar 

  58. Karlin, S, Mrazek, J, and Campbell, AM. (1998) Codon usages in different gene classes of the Escherichia coli genome. Mol. Microbiol. 29, 1341–1355.

    Article  PubMed  CAS  Google Scholar 

  59. Campbell, A, Mrazek, J, and Karlin, S. (1999) Genome signature comparisons among prokaryote, plasmid, and mitochondrial DNA. Proc. Natl. Acad. Sci., USA 96, 9184–9189.

    Article  CAS  Google Scholar 

  60. Mrazek, J, and Karlin, S. (1999) Detecting alien genes in bacterial genomes. Ann. N.Y. Acad. Sci. 870, 314–329.

    Article  CAS  Google Scholar 

  61. Garcia-Vallve, S, Guzman, E, Montero, MA, et al. (2003) HGT-DB: a database of putative horizontally transferred genes in prokaryotic complete genomes. Nucleic Acids Res. 31, 187–189.

    Article  PubMed  CAS  Google Scholar 

  62. Dufraigne, C, Fertil, B, Lespinats, S, et al. (2005) Detection and characterization of horizontal transfers in prokaryotes using genomic signature. Nucleic Acids Res. 33, e6.

    Article  PubMed  Google Scholar 

  63. Chatterjee, R, Chaudhuri, K, and Chaudhuri, P. (2008) On detection and assessment of statistical significance of Genomic Islands. BMC Genomics 9, 150.

    Article  PubMed  Google Scholar 

  64. Tsirigos, A, and Rigoutsos, I. (2005) A sensitive, support-vector-machine method for the detection of horizontal gene transfers in viral, archaeal and bacterial genomes. Nucleic Acids Res. 33, 3699–3707.

    Article  PubMed  CAS  Google Scholar 

  65. Nakamura, Y, Itoh, T, Matsuda, H, et al. (2004) Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat. Genet. 36, 760–766.

    Article  PubMed  CAS  Google Scholar 

  66. Merkl, R. (2004) SIGI: score-based identification of genomic islands. BMC Bioinformatics 5, 22.

    Article  PubMed  Google Scholar 

  67. Vernikos, GS, and Parkhill, J. (2006) Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22, 2196–2203.

    Article  PubMed  CAS  Google Scholar 

  68. Vernikos, GS, and Parkhill, J. (2008) Resolving the structural features of genomic islands: a machine learning approach. Genome Res. 18, 331–342.

    Article  PubMed  CAS  Google Scholar 

  69. Zhang, R, and Zhang, CT. (2005) Genomic Islands in the Corynebacterium efficiens genome. Appl. Environ. Microbiol. 71, 3126–3130.

    Article  PubMed  CAS  Google Scholar 

  70. Sandberg, R, Winberg, G, Branden, CI, et al. (2001) Capturing whole-genome characteristics in short sequences using a naive Bayesian classifier. Genome Res. 11, 1404–1409.

    Article  PubMed  CAS  Google Scholar 

  71. Arvey, AJ, Azad, RK, Raval, A, et al. (2009) Detection of genomic islands via segmental genome heterogeneity. Nucleic Acids Res. 37, 5255–5266.

    Article  PubMed  CAS  Google Scholar 

  72. Médigue, C, Rouxel, T, Vigier, P, et al. (1991) Evidence of horizontal gene transfer in Escherichia coli speciation. J. Mol. Biol. 222, 851–856.

    Article  PubMed  Google Scholar 

  73. Wang, HC, Badger, J, Kearney, P, et al. (2001) Analysis of codon usage patterns of bacterial genomes using the self-organizing map. Mol. Biol. Evol. 18, 792–800.

    Article  PubMed  CAS  Google Scholar 

  74. Kohonen, T. (1982) Self-organized formation of topologically correct feature map. Biol. Cybern. 43, 59–69.

    Article  Google Scholar 

  75. Hayes, WS, and Borodovsky, M. (1998) How to interpret an anonymous bacterial genome: machine learning approach to gene identification. Genome Res. 8, 1154–1171.

    PubMed  CAS  Google Scholar 

  76. Rabiner, L. (1989) A tutorial on Hidden Markov Models and selected applications in speech recognition. Proc. IEEE 77, 257–286.

    Article  Google Scholar 

  77. Azad, RK, and Lawrence, JG. (2007) Detecting laterally transferred genes: use of entropic clustering methods and genome position. Nucleic Acids Res. 35, 4629–4639.

    Article  PubMed  CAS  Google Scholar 

  78. Lin, J. (1991) Divergence measures based on the Shannon entropy. IEEE Trans. Inform. Theory 37, 145–151.

    Article  Google Scholar 

  79. Sandberg, R, Winberg, G, Branden, CI, et al. (2001) Capturing whole-genome characteristics in short sequences using a naive Bayesian classifier. Genome Res 11, 1404–1409.

    Article  PubMed  CAS  Google Scholar 

  80. McHardy, AC, and Rigoutsos, I. (2007) What’s in the mix: phylogenetic classification of metagenome sequence samples. Curr Opin Microbiol 10, 499–503.

    Article  PubMed  CAS  Google Scholar 

  81. McHardy, AC, Martin, HG, Tsirigos, A, et al. (2007) Accurate phylogenetic classification of variable-length DNA fragments. Nat Methods 4, 63–72.

    Article  PubMed  CAS  Google Scholar 

  82. Akaike, H. (1974) A new look at the statistical model identification. IEEE Trans. Automat. Contrl. AC-19, 716–723.

    Google Scholar 

  83. Azad, RK, and Lawrence, JG. (2005) Use of artificial genomes in assessing methods for atypical gene detection. PLoS Comp. Biol. 1, e56.

    Article  Google Scholar 

  84. Braun, JV, and Müller, H-G. (1998) Statistical methods for DNA sequence segmentation. Statistical Science 13, 142–162.

    Article  Google Scholar 

  85. Azad, RK, Lawrence, JG, Thakur, V, et al. (2007) Segmentation of genomic DNA sequences, in Advanced Computational Methods for Biocomputing and Bioimaging (Pham, TD, Yan, H, and Crane, DI, Eds.), Nova Science Publishers, New York.

    Google Scholar 

  86. Durbin, R, Eddy, S, Krogh, A, et al. (1998) Biological Sequence Analysis: Probabilistic models of proteins and nucleic acids, Cambridge University Press, Cambridge.

    Book  Google Scholar 

  87. Bernaola-Galvan, P, Roman-Roldan, R, and Oliver, JL. (1996) Compositional segmentation and long-range fractal correlations in DNA sequences. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 53, 5181–5189.

    Article  PubMed  Google Scholar 

  88. Thakur, V, Azad, RK, and Ramaswamy, R. (2007) Markov models of genome segmentation. Phys Rev E Stat Nonlin Soft Matter Phys 75, 011915.

    Article  PubMed  Google Scholar 

  89. Sueoka, N. (1988) Directional mutation pressure and neutral molecular evolution. Proc. Natl. Acad. Sci., USA 85, 2653–2657.

    Article  CAS  Google Scholar 

  90. Ragan, MA. (2001) On surrogate methods for detecting lateral gene transfer. FEMS Microbiol. Lett. 201, 187–191.

    Article  PubMed  CAS  Google Scholar 

  91. Becq, J, Churlaud, C, and Deschavanne, P. (2010) A benchmark of parametric methods for horizontal transfers detection. PLoS One 5, e9989.

    Article  PubMed  Google Scholar 

  92. Zaneveld, JR, Nemergut, DR, and Knight, R. (2008) Are all horizontal gene transfers created equal? Prospects for mechanism-based studies of HGT patterns. Microbiology 154, 1–15.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by NIH grant GM078092.

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Correspondence to Jeffrey G. Lawrence .

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Azad, R.K., Lawrence, J.G. (2012). Detecting Laterally Transferred Genes. In: Anisimova, M. (eds) Evolutionary Genomics. Methods in Molecular Biology, vol 855. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-61779-582-4_10

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  • DOI: https://doi.org/10.1007/978-1-61779-582-4_10

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