Skip to main content

Horizontal Gene Transfer in Eukaryotic Parasites: A Case Study of Entamoeba histolytica and Trichomonas vaginalis

  • Protocol
Horizontal Gene Transfer

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

Abstract

Over the past few years it has become apparent that horizontal gene transfer (HGT) has played an important role in the evolution of pathogenic prokaryotes. What is less clear is the exact role that HGT has played in shaping the metabolism of eukaryotic organisms. The main problems are the reliable inference of HGT on a genomic scale as well as the functional assignment of genes in these poorly studied organisms. We have screened the completed genomes of the protists Entamoeba histolytica and Trichomonas vaginalis for cases of HGT from prokaryotes. Using a fast primary screen followed by a conservative phylogenetic approach, we found 68 and 153 recent cases of HGT in the respective organisms. The majority of transferred genes that fall into functional categories code for enzymes involved in metabolism. We found a broad range of prokaryotic lineages represented among the donors, but organisms that share similar environmental niches with E. histolytica and T. vaginalis, such as the gut and the vaginal mucosa, dominate.

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. Doolittle, W. F., Boucher, Y., Nesbo, C. L., Douady, C. J., Andersson, J. O., Roger, A. J. (2003) How big is the iceberg of which organellar genes in nuclear genomes are but the tip? Philos Trans R Soc Lond B Biol Sci 358, 39–57.

    Article  CAS  PubMed  Google Scholar 

  2. Koonin, E. V., Makarova, K. S., Aravind, L. (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55, 709–42.

    Article  CAS  PubMed  Google Scholar 

  3. Lawrence, J. G. (2005) Horizontal and vertical gene transfer: the life history of pathogens. Contrib Microbiol 12, 255–71.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  5. Andersson, J. O. (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62, 1182–1197.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Lawrence, J. G. (2005) Common themes in the genome strategies of pathogens. Curr Opin Genet Dev 6, 584–8.

    Article  Google Scholar 

  8. 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 

  9. Andersson, J. O., Sjögren, A. M., Horner, D. S., Murphy, C. A., Dyal, P. L., Svärd, S. G., Logsdon, J. M. Jr, 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. 14, 8–51.

    Google Scholar 

  10. 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  PubMed  Google Scholar 

  11. 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-Saavedr, D., Barton, G. J., Westrop, G. D., Müller, S., Dessi, D., Fiori, P. L., Ren, Q., Paulsen, I., Zhang, H., Bastida-Corcuera, F. D., Simoes-Barbos, 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 

  12. Nanda, N., Michel, R. G., Kurdgelashvili, G., Wendel, K. A. (2006) Trichomoniasis and its treatment. Expert Rev Anti Infect Ther 1, 125–35.

    Article  Google Scholar 

  13. Petri, W. A. Jr., (2000) Protozoan parasites that infect the gastrointestinal tract. Curr Opin Gastroenterol. 1, 18–23.

    Article  Google Scholar 

  14. Shoemaker, N. B., Vlakamis, H., Slyers, A. A. (2001) Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol 67, 561–8.

    Article  CAS  PubMed  Google Scholar 

  15. Sicheritz-Ponten, T., Andersson, S. G. (2001) A phylogenomic approach to microbial evolution. Nucleic Acids Res 29, 545–52

    Article  CAS  PubMed  Google Scholar 

  16. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–402.

    Article  CAS  PubMed  Google Scholar 

  17. Thompson, J. D., Higgins, D. G., Gibson T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–80.

    Article  CAS  PubMed  Google Scholar 

  18. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17, 540–52

    CAS  PubMed  Google Scholar 

  19. Huelsenbeck, J. P., Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–55.

    Article  CAS  PubMed  Google Scholar 

  20. Cummings, M. P., Handley, S. A., Myers, D. S., Reed, D. L., Rokas, A., Winka, K. (2003) Comparing bootstrap and posterior probability values in the four-taxon case. Syst Biol 52, 477–87.

    Article  PubMed  Google Scholar 

  21. Foster, P. G. P4. http://www.bmnh.org/∼pf/p4.html

  22. Desper, R., Gascuel, O. (2004) Theoretical foundation of the balanced minimum evolution method of phylogenetic inference and its relationship to weighted least-squares tree fitting. Mol Biol Evol 21, 587–98.

    Article  CAS  PubMed  Google Scholar 

  23. Timmis, J. N., Ayeliffe, M. A., Huang, C. Y., Martin,W. (2004) Endosymbiotic gene transfers: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5, 123–35.

    Article  CAS  PubMed  Google Scholar 

  24. Rost, B., (1999) Twilight zone of protein sequence alignments. Protein Eng 12, 85–94.

    Article  CAS  PubMed  Google Scholar 

  25. Nair, R., Rost, B. (2002) Sequence conserved for subcellular localization. Protein Sci 11, 2836–47.

    Article  CAS  PubMed  Google Scholar 

  26. Reid, G., Bocking, A. (2003) The potential for probiotics to prevent bacterial vaginosis and preterm labor. Am J Obstet Gynecol. 189, 1202–8.

    Article  PubMed  Google Scholar 

  27. Clark, C. G., Alsmark, U. C. M., Hofer, M., Saito-Nakano,Y., Ali, V., Marion, S., Weber, C., Mukherjee, C., Bruchhaus, I., Tannich, E., Leippe, M., Sicheritz-Ponten, T., Foster, P. G. Samuelson, J., Noél, C. J., Hirt, R. P., Embley, T. M., Gilchrist, C. A., Mann, B. J., Singh, U., Ackers, J. P., Bhattacharya, S., Bhattacharya, A., Lohia, A.,Guillên, N., Duchéne, M., Nozaki, T., Hall, N. (2007) Structure and Content of the Entamoeba histolytica Genome. Adv Parasitol, 65, 51–190.

    Article  CAS  PubMed  Google Scholar 

  28. Andersson, J. O., Doolittle, W. F., Nesbo, C. L. (2001) Genomics. Are there bugs in our genome? Science 292, 1848–50.

    Article  CAS  PubMed  Google Scholar 

  29. Salzberg, S. L., White, O., Peterson, J., Eisen, J. A. (2001) Microbial genes in the human genome: lateral transfer or gene loss? Science 292, 1903–6.

    Article  CAS  PubMed  Google Scholar 

  30. Baldauf, S. L. (2003) The deep roots of eukaryotes. Science 300, 1703–6.

    Article  CAS  PubMed  Google Scholar 

  31. Embley, T. M., Martin, W. (2006) Eukaryotic evolution, changes and challenges. Nature. 440, 623–30.

    Article  CAS  PubMed  Google Scholar 

  32. 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 

  33. 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 

  34. Mira, A., Pushker, R., Legault, B. A., Moreira, D., Rodriguez-Valera, F. (2004) Evolutionary relationships of Fusobacterium nucleatum based on phylogenetic analysis and comparative genomics. BMC Evol Biol 4, 50.

    Article  PubMed  Google Scholar 

  35. Jain, R., Rivera, M. C., Lake, J. A. (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 96, 3801–6.

    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

Alsmark, U.C., Sicheritz-Ponten, T., Foster, P.G., Hirt, R.P., Embley, T.M. (2009). Horizontal Gene Transfer in Eukaryotic Parasites: A Case Study of Entamoeba histolytica and Trichomonas vaginalis. 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_28

Download citation

  • DOI: https://doi.org/10.1007/978-1-60327-853-9_28

  • 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