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Ancient Gene Transfer as a Tool in Phylogenetic Reconstruction

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Horizontal Gene Transfer

Part of the book series: Methods in Molecular Biology ((MIMB,volume 532))

Abstract

Although horizontal gene transfer (HGT) is often considered as a disruptive force in reconstructing organismal phylogeny, it can also be a valuable phylogenetic tool. A gene in the net of life is often horizontally transferred to the ancestor of a major lineage. If the gene is retained in the recipient and its descendants, it will constitute a shared derived character and mark the recipient and all descendants as a monophyletic group. Additionally, phylogenetically informative HGTs also provide information about the sequence of emergence of involved taxa, because the donor organism must have emerged at least as early as the recipient. Here we review the recent applications of ancient HGT events in reconstructing organismal phylogeny as well as the promise and potential pitfalls of this approach.

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References

  1. Hennig, W. (1966) Phylogenetic Systematics, Univ. Illinois Press, Urbana, IL.

    Google Scholar 

  2. Doolittle, W. F. (1999) Phylogenetic classification and the universal tree. Science 284, 2124–9.

    Article  CAS  PubMed  Google Scholar 

  3. Philippe, H., Douady, C. J. (2003) Horizontal gene transfer and phylogenetics. Curr Opin Microbiol 6, 498–505.

    Article  CAS  PubMed  Google Scholar 

  4. Zhaxybayeva, O., Lapierre, P., Gogarten, J. P. (2004) Genome mosaicism and organismal lineages. Trends Genet 20, 254–60.

    Article  CAS  PubMed  Google Scholar 

  5. Keeling, P. J., Burger, G., Durnford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J., Gray, M. W. (2005) The tree of eukaryotes. Trends Ecol Evol 20, 670–6.

    Article  PubMed  Google Scholar 

  6. Parfrey, L. W., Barbero, E., Lasser, E., Dunthorn, M., Bhattacharya, D., Patterson, D. J., Katz, L. A. (2006) Evaluating support for the current classification of eukaryotic diversity. PLoS Genet 2, e220.

    Article  PubMed  Google Scholar 

  7. Kurland, C. G., Canback, B., Berg, O. G. (2003) Horizontal gene transfer: a critical view. Proc Natl Acad Sci U S A 100, 9658–62.

    Article  CAS  PubMed  Google Scholar 

  8. Gogarten, J. P., Doolittle, W. F., Lawrence, J. G. (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19, 2226–38.

    CAS  PubMed  Google Scholar 

  9. Andersson, J. O., Sarchfield, S. W., Roger, A. J. (2005) Gene transfers from nanoarchaeota to an ancestor of diplomonads and parabasalids. Mol Biol Evol 22, 85–90.

    Article  CAS  PubMed  Google Scholar 

  10. Huang, J., Xu, Y., Gogarten, J. P. (2005) The presence of a haloarchaeal type tyrosyl-tRNA synthetase marks the Opisthokonts as monophyletic. Mol Biol Evol 22, 2142–6.

    Article  CAS  PubMed  Google Scholar 

  11. Huang, J., Gogarten, J. P. (2006) Ancient horizontal gene transfer can benefit phylogenetic reconstruction. Trends Genet 22, 361–6.

    Article  CAS  PubMed  Google Scholar 

  12. Rice, D. W., Palmer, J. D. (2006) An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol 4, 31.

    Article  PubMed  Google Scholar 

  13. Woese, C. R. (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci U S A 97, 8392–6.

    Article  CAS  PubMed  Google Scholar 

  14. Lawrence, J. G., Ochman, H. (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A 95, 9413–7.

    Article  CAS  PubMed  Google Scholar 

  15. Hilario, E., Gogarten, J. P. (1993) Horizontal transfer of ATPase genes – the tree of life becomes a net of life. Biosystems 31, 111–9.

    Article  CAS  PubMed  Google Scholar 

  16. Kunin, V., Goldovsky, L., Darzentas, N., Ouzounis, C. A. (2005) The net of life: reconstructing the microbial phylogenetic network. Genome Res 15, 954–9.

    Article  CAS  PubMed  Google Scholar 

  17. Katz, L. A. (1999) The tangled web: gene genealogies and the origin of eukaryotes. Am Nat 154, S137–S45.

    Article  PubMed  Google Scholar 

  18. Andersson, J. O., Roger, A. J. (2003) Evolution of glutamate dehydrogenase genes: evidence for lateral gene transfer within and between prokaryotes and eukaryotes. BMC Evol Biol 3, 14.

    Article  PubMed  Google Scholar 

  19. Huang, J., Mullapudi, N., Sicheritz-Ponten, T., Kissinger, J. C. (2004) A first glimpse into the pattern and scale of gene transfer in Apicomplexa. Int J Parasitol 34, 265–74.

    Article  CAS  PubMed  Google Scholar 

  20. Loftus, B., Anderson, I., Davies, R., Alsmark, U. C., Samuelson, J., Amedeo, P., Roncaglia, P., Berriman, M., Hirt, R. P., Mann, B. J., Nozaki, T., Suh, B., Pop, M., Duchene, M., Ackers, J., Tannich, E., Leippe, M., Hofer, M., Bruchhaus, I., Willhoeft, U., Bhattacharya, A., Chillingworth, T., Churcher, C., Hance, Z., Harris, B., Harris, D., Jagels, K., Moule, S., Mungall, K., Ormond, D., Squares, R., Whitehead, S., Quail, M. A., Rabbinowitsch, E., Norbertczak, H., Price, C., Wang, Z., Guillen, N., Gilchrist, C., Stroup, S. E., Bhattacharya, S., Lohia, A., Foster, P. G., Sicheritz-Ponten, T., Weber, C., Singh, U., Mukherjee, C., El-Sayed, N. M., Petri, W. A., Jr., Clark, C. G., Embley, T. M., Barrell, B., Fraser, C. M., Hall, N. (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433, 865–8.

    Article  CAS  Google Scholar 

  21. Bapteste, E., Boucher, Y., Leigh, J., Doolittle, W. F. (2004) Phylogenetic reconstruction and lateral gene transfer. Trends Microbiol 12, 406–11.

    Article  CAS  PubMed  Google Scholar 

  22. Doolittle, W. F. (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14, 307–11.

    Article  CAS  PubMed  Google Scholar 

  23. Margulis, L. (1995) Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons, W H Freeman & Co, New York.

    Google Scholar 

  24. Gogarten, J. P., Murphey, R. D., nobreak Olendzenski, L. (1999) Horizontal gene transfer: pitfalls and promises. Biol Bull 196, 359–61; discussion 61–2.

    Article  CAS  PubMed  Google Scholar 

  25. Raven, P. H., Evert, R. F., Eichhorn, S. E (1992) Biology of Plants, Worth Publishers, New York.

    Google Scholar 

  26. Palmer, J. D. (2003) The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol 39, 4–11.

    Article  CAS  Google Scholar 

  27. Stiller, J. W., Hall, B. D. (1997) The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci U S A 94, 4520–5.

    Article  CAS  PubMed  Google Scholar 

  28. Rodriguez-Ezpeleta, N., Brinkmann, H., Burey, S. C., Roure, B., Burger, G., Loffelhardt, W., Bohnert, H. J., Philippe, H., Lang, B. F. (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15, 1325–30.

    Article  CAS  PubMed  Google Scholar 

  29. Nozaki, H., Iseki, M., Hasegawa, M., Misawa, K., Nakada, T., Sasaki, N., Watanabe, M. (2007) Phylogeny of primary photosynthetic eukaryotes as deduced from slowly evolving nuclear genes. Mol Biol Evol 24, 1592–5.

    Article  CAS  PubMed  Google Scholar 

  30. Reyes-Prieto, A., Bhattacharya, D. (2007) Phylogeny of Calvin cycle enzymes supports plantae monophyly. Mol Phylogenet Evol 45, 384–91.

    Article  CAS  PubMed  Google Scholar 

  31. Stiller, J. W. (2007) Plastid endosymbiosis, genome evolution and the origin of green plants. Trends Plant Sci 12, 391–6.

    Article  CAS  PubMed  Google Scholar 

  32. Richards, T. A., Dacks, J. B., Campbell, S. A., Blanchard, J. L., Foster, P. G., Mcleod, R., Roberts, C. W. (2006) Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot Cell 5, 1517–31.

    Article  CAS  PubMed  Google Scholar 

  33. Huang, J., Gogarten, P. (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8, R99.

    Article  PubMed  Google Scholar 

  34. Tyra, H. M., Linka, M., Weber, A. P., Bhattacharya, D. (2007) Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8, R212.

    Article  PubMed  Google Scholar 

  35. Brinkman, F. S., Blanchard, J. L., Cherkasov, A., Av-Gay, Y., Brunham, R. C., Fernandez, R. C., Finlay, B. B., Otto, S. P., Ouellette, B. F., Keeling, P. J., Rose, A. M., Hancock, R. E., Jones, S. J., Greberg, H. (2002) Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res 12, 1159–67.

    Article  CAS  PubMed  Google Scholar 

  36. Douglas, S., Zauner, S., Fraunholz, M., Beaton, M., Penny, S., Deng, L. T., Wu, X., Reith, M., Cavalier-Smith, T., Maier, U. G. (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410, 1091–6.

    Article  CAS  PubMed  Google Scholar 

  37. Cavalier-Smith, T., Allsopp, M. T., Chao, E. E. (1994) Chimeric conundra: are nucleomorphs and chromists monophyletic or polyphyletic? Proc Natl Acad Sci U S A 91, 11368–72.

    Article  CAS  PubMed  Google Scholar 

  38. Yoon, H. S., Hackett, J. D., Pinto, G., Bhattacharya, D. (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci U S A 99, 15507–12.

    Article  CAS  PubMed  Google Scholar 

  39. Bachvaroff, T. R., Sanchez Puerta, M. V., Delwiche, C. F. (2005) Chlorophyll c-containing plastid relationships based on analyses of a multigene data set with all four chromalveolate lineages. Mol Biol Evol 22, 1772–82.

    Article  CAS  PubMed  Google Scholar 

  40. Lang, B. F., Gray, M. W., Burger, G. (1999) Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet 33, 351–97.

    Article  CAS  PubMed  Google Scholar 

  41. Hackett, J. D., Yoon, H. S., Li, S., Reyes-Prieto, A., Rummele, S. E., Bhattacharya, D. (2007) Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol 24, 1702–13.

    Article  CAS  PubMed  Google Scholar 

  42. Patron, N. J., Inagaki, Y., Keeling, P. J. (2007) Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr Biol 17, 887–91.

    Article  CAS  PubMed  Google Scholar 

  43. Zhaxybayeva, O., Gogarten, J. P., Charlebois, R. L., Doolittle, W. F., Papke, R. T. (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16, 1099–108.

    Article  CAS  PubMed  Google Scholar 

  44. Beiko, R. G., Harlow, T. J., Ragan, M. A. (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102, 14332–7.

    Article  CAS  PubMed  Google Scholar 

  45. Ting, C. S., Rocap, G., King, J., Chisholm, S. W. (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol 10, 134–42.

    Article  CAS  PubMed  Google Scholar 

  46. Partensky, F., Hess, W. R., Vaulot, D. (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63, 106–27.

    CAS  PubMed  Google Scholar 

  47. Hannaert, V., Saavedra, E., Duffieux, F., Szikora, J. P., Rigden, D. J., Michels, P. A., Opperdoes, F. R. (2003) Plant-like traits associated with metabolism of Trypanosoma parasites. Proc Natl Acad Sci U S A 100, 1067–71.

    Article  CAS  PubMed  Google Scholar 

  48. Huang, J., Mullapudi, N., Lancto, C. A., Scott, M., Abrahamsen, M. S., Kissinger, J. C. (2004) Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol 5, R88.

    Google Scholar 

  49. Rogers, M., Keeling, P. J. (2004) Lateral transfer and recompartmentalization of Calvin cycle enzymes of plants and algae. J Mol Evol 58, 367–75.

    Article  CAS  PubMed  Google Scholar 

  50. El-Sayed, N. M., Myler, P. J., Blandin, G., Berriman, M., Crabtree, J., Aggarwal, G., Caler, E., Renauld, H., Worthey, E. A., Hertz-Fowler, C., Ghedin, E., Peacock, C., Bartholomeu, D. C., Haas, B. J., Tran, A. N., Wortman, J. R., Alsmark, U. C., Angiuoli, S., Anupama, A., Badger, J., Bringaud, F., Cadag, E., Carlton, J. M., Cerqueira, G. C., Creasy, T., Delcher, A. L., Djikeng, A., Embley, T. M., Hauser, C., Ivens, A. C., Kummerfeld, S. K., Pereira-Leal, J. B., Nilsson, D., Peterson, J., Salzberg, S. L., Shallom, J., Silva, J. C., Sundaram, J., Westenberger, S., White, O., Melville, S. E., Donelson, J. E., Andersson, B., Stuart, K. D., Hall, N. (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309, 404–9.

    Article  CAS  PubMed  Google Scholar 

  51. Gogarten, J. P., Townsend, J. P. (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3, 679–87.

    Article  CAS  PubMed  Google Scholar 

  52. Andersson, J. O., Sjogren, A. M., Davis, L. A., Embley, T. M., Roger, A. J. (2003) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13, 94–104.

    Article  CAS  PubMed  Google Scholar 

  53. Richards, T. A., Dacks, J. B., Jenkinson, J. M., Thornton, C. R., Talbot, N. J. (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 16, 1857–64.

    Article  CAS  PubMed  Google Scholar 

  54. Nosenko, T., Bhattacharya, D. (2007) Horizontal gene transfer in chromalveolates. BMC Evol Biol 7, 173.

    Article  PubMed  Google Scholar 

  55. Bapteste, E., Brinkmann, H., Lee, J. A., Moore, D. V., Sensen, C. W., Gordon, P., Durufle, L., Gaasterland, T., Lopez, P., Muller, M., Philippe, H. (2002) The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc Natl Acad Sci U S A 99, 1414–9.

    Article  CAS  PubMed  Google Scholar 

  56. Rodriguez-Ezpeleta, N., Brinkmann, H., Burger, G., Roger, A. J., Gray, M. W., Philippe, H., Lang, B. F. (2007) Toward resolving the eukaryotic tree: the phylogenetic positions of jakobids and cercozoans. Curr Biol 17, 1420–5.

    Article  CAS  PubMed  Google Scholar 

  57. Guindon, S., Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.

    Article  PubMed  Google Scholar 

  58. Felsenstein, J. (2005) PHYLIP (Phylogeny Inference Package) Version 3.65. Distributed by the author. Department of Genome Sciences, University of Washington Place, Seattle, WA.

    Google Scholar 

  59. Ronquist, F., Huelsenbeck, J. P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–4.

    Article  CAS  PubMed  Google Scholar 

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Huang, J., Gogarten, J.P. (2009). Ancient Gene Transfer as a Tool in Phylogenetic Reconstruction. In: Gogarten, M.B., Gogarten, J.P., Olendzenski, L.C. (eds) Horizontal Gene Transfer. Methods in Molecular Biology, vol 532. Humana Press. https://doi.org/10.1007/978-1-60327-853-9_7

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  • DOI: https://doi.org/10.1007/978-1-60327-853-9_7

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60327-852-2

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