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.
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References
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.
Koonin, E. V., Makarova, K. S., Aravind, L. (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55, 709–42.
Lawrence, J. G. (2005) Horizontal and vertical gene transfer: the life history of pathogens. Contrib Microbiol 12, 255–71.
Ochman, H., Lawrence, J. G., Groisman, E. A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304.
Andersson, J. O. (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62, 1182–1197.
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.
Lawrence, J. G. (2005) Common themes in the genome strategies of pathogens. Curr Opin Genet Dev 6, 584–8.
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.
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.
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.
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.
Nanda, N., Michel, R. G., Kurdgelashvili, G., Wendel, K. A. (2006) Trichomoniasis and its treatment. Expert Rev Anti Infect Ther 1, 125–35.
Petri, W. A. Jr., (2000) Protozoan parasites that infect the gastrointestinal tract. Curr Opin Gastroenterol. 1, 18–23.
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.
Sicheritz-Ponten, T., Andersson, S. G. (2001) A phylogenomic approach to microbial evolution. Nucleic Acids Res 29, 545–52
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.
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.
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17, 540–52
Huelsenbeck, J. P., Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–55.
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.
Foster, P. G. P4. http://www.bmnh.org/∼pf/p4.html
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.
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.
Rost, B., (1999) Twilight zone of protein sequence alignments. Protein Eng 12, 85–94.
Nair, R., Rost, B. (2002) Sequence conserved for subcellular localization. Protein Sci 11, 2836–47.
Reid, G., Bocking, A. (2003) The potential for probiotics to prevent bacterial vaginosis and preterm labor. Am J Obstet Gynecol. 189, 1202–8.
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.
Andersson, J. O., Doolittle, W. F., Nesbo, C. L. (2001) Genomics. Are there bugs in our genome? Science 292, 1848–50.
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.
Baldauf, S. L. (2003) The deep roots of eukaryotes. Science 300, 1703–6.
Embley, T. M., Martin, W. (2006) Eukaryotic evolution, changes and challenges. Nature. 440, 623–30.
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.
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.
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.
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.
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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
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DOI: https://doi.org/10.1007/978-1-60327-853-9_28
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