Journal of Molecular Evolution

, Volume 63, Issue 6, pp 801–814 | Cite as

The Frequency of Eubacterium-to-Eukaryote Lateral Gene Transfers Shows Significant Cross-Taxa Variation Within Amoebozoa



Single-celled bacterivorous eukaryotes offer excellent test cases for evaluation of the frequency of prey-to-predator lateral gene transfer (LGT). Here we use analysis of expressed sequence tag (EST) data sets to quantify the extent of LGT from eubacteria to two amoebae, Acanthamoeba castellanii and Hartmannella vermiformis. Stringent screening for LGT proceeded in several steps intended to enrich for authentic events while at the same time minimizing the incidence of false positives due to factors such as limitations in database coverage and ancient paralogy. The results were compared with data obtained when the same methodology was applied to EST libraries from a number of other eukaryotic taxa. Significant differences in the extent of apparent eubacterium-to-eukaryote LGT were found between taxa. Our results indicate that there may be substantial inter-taxon variation in the number of LGT events that become fixed even between amoebozoan species that have similar feeding modalities.


Lateral gene transfer Horizontal gene transfer Eukaryotes Eubacteria Genome evolution Amoebozoa Acanthamoeba Hartmannella Dictyostelium Expressed sequence tags 



We thank C. Nesbø for her careful reading of the original draft of the manuscript and for her insightful comments. We also thank A. Roger for very useful discussions. This study was conducted under the auspices of the Protist EST Program (PEP), a Genome Canada large-scale genomics project, with funding through Genome Atlantic and the Atlantic Innovation Fund. M.W.G. is pleased to acknowledge salary support from the Canada Research Chairs Program and the Canadian Institute for Advanced Research (Program in Evolutionary Biology).

Supplementary material

suppA.doc (233 kb)
Supplementary material 1
suppB.doc (36 kb)
Supplementary material 2
suppC.doc (175 kb)
Supplementary material 3 (282 kb)
Supplementary material 4


  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. Anderson IJ, Watkins RF, Samuelson J, Spencer DF, Majoros WH, Gray MW, Loftus BJ (2005) Gene discovery in the Acanthamoeba castellanii genome. Protist 156:203–214PubMedCrossRefGoogle Scholar
  3. Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62:1182–1197PubMedCrossRefGoogle Scholar
  4. Andersson JO, Roger AJ (2002) Evolutionary analyses of the small subunit of glutamate synthase: gene order conservation, gene fusions, and prokaryote-to-eukaryote lateral gene transfers. Eukaryot Cell 1:304–310PubMedCrossRefGoogle Scholar
  5. Andersson JO, Roger AJ (2003) Evolution of glutamate dehydrogenase genes: evidence for lateral gene transfer within and between prokaryotes and eukaryotes. BMC Evol Biol 3:14PubMedCrossRefGoogle Scholar
  6. Andersson JO, Doolittle WF, Nesbø CL (2001) Are there bugs in our genome? Science 292:1848–1850PubMedCrossRefGoogle Scholar
  7. Andersson JO, Sjögren ÅM, Davis LAM, Embley TM, Roger AJ (2003) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13:94–104PubMedCrossRefGoogle Scholar
  8. Andersson JO, Sarchfield SW, Roger AJ (2005) Gene transfers from Nanoarchaeota to an ancestor of diplomonads and parabasalids. Mol Biol Evol 22:85–90PubMedCrossRefGoogle Scholar
  9. Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ (2003) Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci USA 100:7678–7683PubMedCrossRefGoogle Scholar
  10. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500PubMedCrossRefGoogle Scholar
  11. Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311PubMedCrossRefGoogle Scholar
  12. Doolittle WF (1999) Lateral genomics. Trends Cell Biol 1999:M5–M8CrossRefGoogle Scholar
  13. Doolittle WF, Boucher Y, Nesbø CL, Douady CJ, Andersson JO, Roger AJ (2002) How big is the iceberg of which organellar genes in nuclear genomes are but the tip? Philos Trans R Soc Lond B Biol Sci 358:39–58CrossRefGoogle Scholar
  14. Eichinger L, Pachebat JA, Glöckner G, Rajandream M-A, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57PubMedCrossRefGoogle Scholar
  15. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–178PubMedGoogle Scholar
  16. Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (version 3.2). Cladistics 5:164–166Google Scholar
  17. Figge RM, Schubert M, Brinkmann H, Cerff R (1999) Glyceraldehyde-3-phosphate dehydrogenase gene diversity in eubacteria and eukaryotes: evidence for intra- and inter-kingdom gene transfer. Mol Biol Evol 16:429–440PubMedGoogle Scholar
  18. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548PubMedGoogle Scholar
  19. Hall C, Brachat S, Dietrich FS (2005) Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot Cell 4:1102–1115PubMedCrossRefGoogle Scholar
  20. Harper JT, Keeling PJ (2004) Lateral gene transfer and the complex distribution of insertions in eukaryotic enolase. Gene 340:227–235PubMedCrossRefGoogle Scholar
  21. Horn M, Wagner M (2004) Bacterial endosymbionts of free-living amoebae. J Euk Microbiol 51:509–514PubMedCrossRefGoogle Scholar
  22. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877PubMedCrossRefGoogle Scholar
  23. Huang J, Mullapudi N, Lancto CA, Scott M, Abrahamsen MS, Kissinger JC (2004) Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol 5:R88PubMedCrossRefGoogle Scholar
  24. Jeon KW (2004) Genetic and physiological interactions in the amoeba-bacteria symbiosis. J Eukaryot Microbiol 51:502–508PubMedCrossRefGoogle Scholar
  25. Katz LA (2002) Lateral gene transfers and the evolution of eukaryotes: theories and data. Int J Syst Evol Microbiol 52:1893–1900PubMedCrossRefGoogle Scholar
  26. Keeling PJ, 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 USA 101:15380–15385PubMedCrossRefGoogle Scholar
  27. Keeling PJ, Palmer JD (2001) Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase. Proc Natl Acad Sci USA 98:10745–10750PubMedCrossRefGoogle Scholar
  28. Koonin EV, Makarova KS, Aravind L (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55:709–742PubMedCrossRefGoogle Scholar
  29. Kuiper MW, Wullings BA, Akkermans AD, Beumer RR, van der Kooij D (2004) Intracellular proliferation of Legionella pneumophila in Hartmannella vermiformis in aquatic biofilms grown on plasticized polyvinyl chloride. Appl Environ Microbiol 70:6826–6833PubMedCrossRefGoogle Scholar
  30. Kurland CG (2005) What tangled web: barriers to rampant horizontal gene transfer. Bioessays 27:741–747PubMedCrossRefGoogle Scholar
  31. Lander ES, Linton LM, Birren B, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedCrossRefGoogle Scholar
  32. Loftus B, Anderson I, Davies R, Alsmark UCM, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, 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 MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillén N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, El-Sayed NM, Petri WA Jr, Clark CG, Embley TM, Barrell B, Fraser CM, Hall N (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433:865–868PubMedCrossRefGoogle Scholar
  33. Neff RJ, Ray SA, Benton WF, Wilborn M (1964) Induction of synchronous encystment (differentiation) in Acanthamoeba sp. In: Prescott DM (ed) Methods in cell physiology, Vol I. Academic Press, New York, pp 55–83Google Scholar
  34. Qian Q, Keeling PJ (2001) Diplonemid glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and prokaryote-to-eukaryote lateral gene transfer. Protist 152:193–201PubMedCrossRefGoogle Scholar
  35. Salzberg SL, White O, Peterson J, Eisen JA (2001) Microbial genes in the human genome: lateral transfer or gene loss? Science 292:1903–1906PubMedCrossRefGoogle Scholar
  36. Schlieper D, Oliva MA, Andreu JM, Löwe J (2005) Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc Natl Acad Sci USA 102:9170–9175PubMedCrossRefGoogle Scholar
  37. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504PubMedCrossRefGoogle Scholar
  38. Sicheritz-Pontén T, Andersson SGE (2001) A phylogenomic approach to microbial evolution. Nucleic Acids Res 29:545–552PubMedCrossRefGoogle Scholar
  39. Simpson AG, Roger AJ (2004) The real ‘kingdoms’ of eukaryotes. Curr Biol 14:R693–R696PubMedCrossRefGoogle Scholar
  40. Stanhope MJ, Lupas A, Italia MJ, Koretke KK, Volker C, Brown JR (2001) Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411:940–944PubMedCrossRefGoogle Scholar
  41. Zardoya R, Ding X, Kitagawa Y, Chrispeels MJ (2002) Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc Natl Acad Sci USA 99:14893–14896PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Centre for Molecular Medicine and Therapeutics, Child & Family Research Institute, and Department of Medical GeneticsUniversity of British ColumbiaVancouverCanada
  2. 2.Department of Biochemistry and Molecular BiologyDalhousie UniversityHalifaxCanada

Personalised recommendations