Skip to main content

Horizontal Gene Transfer Between Microbial Eukaryotes

  • Protocol
Horizontal Gene Transfer

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

Abstract

Comparative genomics have identified two loosely defined classes of genes: widely distributed core genes that encode proteins for central functions in the cell and accessory genes that are patchily distributed across lineages and encode taxa-specific functions. Studies of microbial eukaryotes show that both categories undergo horizontal gene transfer (HGT) from prokaryotes, but also between eukaryotic organisms. Intra-domain gene transfers of most core genes seem to be relatively infrequent and therefore comparatively easy to detect using phylogenetic methods. In contrast, phylogenies of accessory genes often have complex topologies with little or no resemblance of organismal relationships typically with eukaryotes and prokaryotes intermingled, making detailed evolutionary histories difficult to interpret. Nevertheless, this suggests significant rates of gene transfer between and among the three domains of life for many of these genes, affecting a considerably diversity of eukaryotic microbes, although the current depth of taxonomic sampling usually is insufficient to pin down individual transfer events. The occurrence of intra-domain transfer among microbial eukaryotes has important implications for studies of organismal phylogeny as well as eukaryote genome evolution in general.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Boucher, Y., Douady, C. J., Papke, R. T., Walsh, D. A., Boudreau, M. E. R., Nesbø, C. L., Case, R. J., Doolittle, W. F. (2003) Lateral gene transfer and the origins of prokaryotic groups. Annu Rev Genet 37, 283–328.

    Article  CAS  PubMed  Google Scholar 

  2. 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 

  3. Andersson, J. O., Sjögren, Å. M., Davis, L. A. M., 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 

  4. 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.

    Article  PubMed  Google Scholar 

  5. Loftus, B., Anderson, I., Davies, R., Alsmark, U. C. M., 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  PubMed  Google Scholar 

  6. Ricard, G., Mcewan, N. R., Dutilh, B. E., Jouany, J. P., Macheboeuf, D., Mitsumori, M., Mcintosh, F. M., Michalowski, T., Nagamine, T., Nelson, N., Newbold, C. J., Nsabimana, E., Takenaka, A., Thomas, N. A., Ushida, K., Hackstein, J. H., Huynen, M. A. (2006) Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic carbohydrates rich environment. BMC Genomics 7, 22.

    Article  PubMed  Google Scholar 

  7. Carlton, J. M., Hirt, R. P., Silva, J. C., Delcher, A. L., Schatz, M., Zhao, Q., Wortman, J. R., Bidwell, S. L., Alsmark, U. C., Besteiro, S., Sicheritz-Ponten, T., Noel, C. J., Dacks, J. B., Foster, P. G., Simillion, C., Van De Peer, Y., Miranda-Saavedra, D., Barton, G. J., Westrop, G. D., Muller, S., Dessi, D., Fiori, P. L., Ren, Q., Paulsen, I., Zhang, H., Bastida-Corcuera, F. D., Simoes-Barbosa, A., Brown, M. T., Hayes, R. D., Mukherjee, M., Okumura, C. Y., Schneider, R., Smith, A. J., Vanacova, S., Villalvazo, M., Haas, B. J., Pertea, M., Feldblyum, T. V., Utterback, T. R., Shu, C. L., Osoegawa, K., De Jong, P. J., Hrdy, I., Horvathova, L., Zubacova, Z., Dolezal, P., Malik, S. B., Logsdon, J. M., Jr., Henze, K., Gupta, A., Wang, C. C., Dunne, R. L., Upcroft, J. A., Upcroft, P., White, O., Salzberg, S. L., Tang, P., Chiu, C. H., Lee, Y. S., Embley, T. M., Coombs, G. H., Mottram, J. C., Tachezy, J., Fraser-Liggett, C. M., Johnson, P. J. (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315, 207–12.

    Article  PubMed  Google Scholar 

  8. Andersson, J. O., Sjögren, Å. M., Horner, D. S., Murphy, C. A., Dyal, P. L., Svärd, S. G., Logsdon Jr, J. M., Ragan, M. A., Hirt, R. P., Roger, A. J. (2007) A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC Genomics 8, 51.

    Article  PubMed  Google Scholar 

  9. Richardson, A. O., Palmer, J. D. (2006) Horizontal gene transfer in plants. J Exp Bot 58, 1–9.

    Article  PubMed  Google Scholar 

  10. Scholl, E. H., Thorne, J. L., Mccarter, J. P., Bird, D. M. (2003) Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4, R39.

    Article  PubMed  Google Scholar 

  11. Hotopp, J. C., Clark, M. E., Oliveira, D. C., Foster, J. M., Fischer, P., Torres, M. C., Giebel, J. D., Kumar, N., Ishmael, N., Wang, S., Ingram, J., Nene, R. V., Shepard, J., Tomkins, J., Richards, S., Spiro, D. J., Ghedin, E., Slatko, B. E., Tettelin, H., Werren, J. H. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–6.

    Article  Google Scholar 

  12. Andersson, J. O. (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62, 1182–97.

    Article  CAS  PubMed  Google Scholar 

  13. 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 

  14. Ciccarelli, F. D., Doerks, T., Von Mering, C., Creevey, C. J., Snel, B., Bork, P. (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283–7.

    Article  CAS  PubMed  Google Scholar 

  15. Charlebois, R. L., Doolittle, W. F. (2004) Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res 14, 2469–77.

    Article  CAS  PubMed  Google Scholar 

  16. Lerat, E., Daubin, V., Ochman, H., Moran, N. A. (2005) Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3, e130.

    Article  PubMed  Google Scholar 

  17. Kettler, G. C., Martiny, A. C., Huang, K., Zucker, J., Coleman, M. L., Rodrigue, S., Chen, F., Lapidus, A., Ferriera, S., Johnson, J., Steglich, C., Church, G. M., Richardson, P., Chisholm, S. W. (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3, e231.

    Article  PubMed  Google Scholar 

  18. Welch, R. A., Burland, V., Plunkett, G., 3rd, Redford, P., Roesch, P., Rasko, D., Buckles, E. L., Liou, S. R., Boutin, A., Hackett, J., Stroud, D., Mayhew, G. F., Rose, D. J., Zhou, S., Schwartz, D. C., Perna, N. T., Mobley, H. L., Donnenberg, M. S., Blattner, F. R. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99, 17020–4.

    Article  CAS  PubMed  Google Scholar 

  19. Keeling, P. J., Inagaki, Y. (2004) A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1α. Proc Natl Acad Sci U S A 101, 15380–5.

    Article  CAS  PubMed  Google Scholar 

  20. Ruiz-Trillo, I., Lane, C. E., Archibald, J. M., Roger, A. J. (2006) Insights into the evolutionary origin and genome architecture of the unicellular opisthokonts Capsaspora owczarzaki and Sphaeroforma arctica. J Eukaryot Microbiol 53, 379–84.

    Article  CAS  PubMed  Google Scholar 

  21. Noble, G. P., Rogers, M. B., Keeling, P. J. (2007) Complex distribution of EFL and EF-1alpha proteins in the green algal lineage. BMC Evol Biol 7, 82.

    Article  PubMed  Google Scholar 

  22. Gile, G. H., Patron, N. J., Keeling, P. J. (2006) EFL GTPase in cryptomonads and the distribution of EFL and EF-1α in chromalveolates. Protist 157, 435–44.

    Article  CAS  PubMed  Google Scholar 

  23. Simpson, A. G. B., Perley, T. A., Lara, E. (2008) Lateral transfer of the gene for a widely used marker, alpha-tubulin, indicated by a multi-protein study of the phylogenetic position of Andalucia (Excavata). Mol Phylogenet Evol in press.

    Google Scholar 

  24. Lara, E., Chatzinotas, A., Simpson, A. G. (2006) Andalucia (n. gen.) – the deepest branch within jakobids (Jakobida; Excavata), based on morphological and molecular study of a new flagellate from soil. J Eukaryot Microbiol 53, 112–20.

    Article  CAS  PubMed  Google Scholar 

  25. 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 

  26. 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 

  27. Rogers, M. B., Watkins, R. F., Harper, J. T., Durnford, D. G., Gray, M. W., Keeling, P. J. (2007) A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evol Biol 7, 89.

    Article  PubMed  Google Scholar 

  28. Fothergill-Gilmore, L. A., Michels, P. A. (1993) Evolution of glycolysis. Prog Biophys Mol Biol 59, 105–235.

    Article  CAS  PubMed  Google Scholar 

  29. Liapounova, N. A., Hampl, V., Gordon, P. M., Sensen, C. W., Gedamu, L., Dacks, J. B. (2006) Reconstructing the mosaic glycolytic pathway of the anaerobic eukaryote Monocercomonoides. Eukaryot Cell 5, 2138–46.

    Article  CAS  PubMed  Google Scholar 

  30. Stechmann, A., Baumgartner, M., Silberman, J. D., Roger, A. J. (2006) The glycolytic pathway of Trimastix pyriformis is an evolutionary mosaic. BMC Evol Biol 6, 101.

    Article  PubMed  Google Scholar 

  31. Andersson, J. O. (2006) Genome evolution of anaerobic protists: metabolic adaptation via gene acquisition, in Genomics and Evolution of Microbial Eukaryotes (Katz, L. A., Bhattacharya D., ed.) Oxford University Press, Oxford 109–22.

    Google Scholar 

  32. Hampl, V., Silberman, J. D., Stechmann, A., Diaz-Trivino, S., Johnson, P. J., Roger, A. J. (2008) Genetic evidence for a mitochondriate ancestry in the ‘amitochondriate’ flagellate Trimastix pyriformis. PLoS ONE 3, e1383.

    Article  PubMed  Google Scholar 

  33. Adl, S. M., Simpson, A. G., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., Bowser, S. S., Brugerolle, G., Fensome, R. A., Fredericq, S., James, T. Y., Karpov, S., Kugrens, P., Krug, J., Lane, C. E., Lewis, L. A., Lodge, J., Lynn, D. H., Mann, D. G., Mccourt, R. M., Mendoza, L., Moestrup, O., Mozley-Standridge, S. E., Nerad, T. A., Shearer, C. A., Smirnov, A. V., Spiegel, F. W., Taylor, M. F. (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52, 399–451.

    Article  PubMed  Google Scholar 

  34. Rosewich, U. L., Kistler, H. C. (2000) Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38, 325–63.

    Article  CAS  PubMed  Google Scholar 

  35. Walton, J. D. (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30, 167–71.

    Article  CAS  PubMed  Google Scholar 

  36. Patron, N. J., Waller, R. F., Cozijnsen, A. J., Straney, D. C., Gardiner, D. M., Nierman, W. C., Howlett, B. J. (2007) Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol Biol 7, 174.

    Article  PubMed  Google Scholar 

  37. Khaldi, N., Collemare, J., Lebrun, M. H., Wolfe, K. H. (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9, R18.

    Article  PubMed  Google Scholar 

  38. Temporini, E. D., Vanetten, H. D. (2004) An analysis of the phylogenetic distribution of the pea pathogenicity genes of Nectria haematococca MPVI supports the hypothesis of their origin by horizontal transfer and uncovers a potentially new pathogen of garden pea: Neocosmospora boniensis. Curr Genet 46, 29–36.

    Article  CAS  PubMed  Google Scholar 

  39. Slot, J. C., Hibbett, D. S. (2007) Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS ONE 2, e1097.

    Article  PubMed  Google Scholar 

  40. Friesen, T. L., Stukenbrock, E. H., Liu, Z., Meinhardt, S., Ling, H., Faris, J. D., Rasmussen, J. B., Solomon, P. S., Mcdonald, B. A., Oliver, R. P. (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38, 953–6.

    Article  CAS  PubMed  Google Scholar 

  41. Inderbitzin, P., Harkness, J., Turgeon, B. G., Berbee, M. L. (2005) Lateral transfer of mating system in Stemphylium. Proc Natl Acad Sci U S A 102, 11390–5.

    Article  CAS  PubMed  Google Scholar 

  42. Fitzpatrick, D. A., Logue, M. E., Stajich, J. E., Butler, G. (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6, 99.

    Article  PubMed  Google Scholar 

  43. Latijnhouwers, M., De Wit, P. J., Govers, F. (2003) Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol 11, 462–9.

    Article  CAS  PubMed  Google Scholar 

  44. Belbahri, L., Calmin, G., Mauch, F., Andersson, J. O. (2008) Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 408, 1–8.

    Article  CAS  PubMed  Google Scholar 

  45. Kolattukudy, P. E., Rogers, L. M., Li, D., Hwang, C. S., Flaishman, M. A. (1995) Surface signaling in pathogenesis. Proc Natl Acad Sci U S A 92, 4080–7.

    Article  CAS  PubMed  Google Scholar 

  46. Kenrick, P., Crane, P. R. (1997) The origin and early evolution of plants on land. Nature 389, 33–9.

    Article  CAS  Google Scholar 

  47. Smith, M. W., Feng, D. F., Doolittle, R. F. (1992) Evolution by acquisition: the case for horizontal gene transfers. Trends Biochem Sci 17, 489–93.

    Article  CAS  PubMed  Google Scholar 

  48. Yooseph, S., Sutton, G., Rusch, D. B., Halpern, A. L., Williamson, S. J., Remington, K., Eisen, J. A., Heidelberg, K. B., Manning, G., Li, W., Jaroszewski, L., Cieplak, P., Miller, C. S., Li, H., Mashiyama, S. T., Joachimiak, M. P., Van Belle, C., Chandonia, J. M., Soergel, D. A., Zhai, Y., Natarajan, K., Lee, S., Raphael, B. J., Bafna, V., Friedman, R., Brenner, S. E., Godzik, A., Eisenberg, D., Dixon, J. E., Taylor, S. S., Strausberg, R. L., Frazier, M., Venter, J. C. (2007) The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol 5, e16.

    Article  PubMed  Google Scholar 

  49. Canbäck, B., Andersson, S. G. E., Kurland, C. G. (2002) The global phylogeny of glycolytic enzymes. Proc Natl Acad Sci U S A 99, 6097–102.

    Article  PubMed  Google Scholar 

  50. Andersson, J. O., Hirt, R. P., Foster, P. G., Roger, A. J. (2006) Evolution of four gene families with patchy phylogenetic distribution: influx of genes into protist genomes. BMC Evol Biol 6, 27.

    Article  PubMed  Google Scholar 

  51. Richards, T. A., Hirt, R. P., Williams, B. A., Embley, T. M. (2003) Horizontal gene transfer and the evolution of parasitic protozoa. Protist 154, 17–32.

    Article  PubMed  Google Scholar 

  52. Dyall, S. D., Yan, W., Delgadillo-Correa, M. G., Lunceford, A., Loo, J. A., Clarke, C. F., Johnson, P. J. (2004) Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431, 1103–7.

    Article  CAS  PubMed  Google Scholar 

  53. Hrdy, I., Hirt, R. P., Dolezal, P., Bardonova, L., Foster, P. G., Tachezy, J., Embley, T. M. (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432, 618–22.

    Article  CAS  PubMed  Google Scholar 

  54. 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 

  55. Baldauf, S. L., Roger, A. J., Wenk-Siefert, I., Doolittle, W. F. (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290, 972–7.

    Article  CAS  PubMed  Google Scholar 

  56. Delsuc, F., Brinkmann, H., Philippe, H. (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6, 361–75.

    Article  CAS  PubMed  Google Scholar 

  57. Leigh, J. W., Susko, E., Baumgartner, M., Roger, A. J. (2008) Testing congruence in phylogenomic analysis. Syst Biol 57, 104–15.

    Article  PubMed  Google Scholar 

  58. Planet, P. J. (2006) Tree disagreement: measuring and testing incongruence in phylogenies. J Biomed Inform 39, 86–102.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Andersson, J.O. (2009). Horizontal Gene Transfer Between Microbial Eukaryotes. 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_27

Download citation

  • DOI: https://doi.org/10.1007/978-1-60327-853-9_27

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60327-852-2

  • Online ISBN: 978-1-60327-853-9

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics