Abstract
We discuss the impact of horizontal gene transfer (HGT) on phylogenetic reconstruction and taxonomy. We review the power of HGT as a creative force in assembling new metabolic pathways, and we discuss the impact that HGT has on phylogenetic reconstruction. On one hand, shared derived characters are created through transferred genes that persist in the recipient lineage, either because they were adaptive in the recipient lineage or because they resulted in a functional replacement. On the other hand, taxonomic patterns in microbial phylogenies might also be created through biased gene transfer. The agreement between different molecular phylogenies has encouraged interpretation of the consensus signal as reflecting organismal history or as the tree of cell divisions; however, to date the extent to which the consensus reflects shared organismal ancestry and to which it reflects highways of gene sharing and biased gene transfer remains an open question. Preferential patterns of gene exchange act as a homogenizing force in creating and maintaining microbial groups, generating taxonomic patterns that are indistinguishable to those created by shared ancestry. To understand the evolution of higher bacterial taxonomic units, concepts usually applied in population genetics need to be applied.
Similar content being viewed by others
References
Acinas SG, Marcelino LA, Klepac-Ceraj V, Polz MF (2004) Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186:2629–2635
Adams KL, Song K, Roessler PG, Nugent JM, Doyle JL, Doyle JJ, Palmer JD (1999) Intracellular gene transfer in action: dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes. Proc Natl Acad Sci U S A 96:13863–13868
Asai T, Zaporojets D, Squires C, Squires CL (1999) An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria [see comments]. Proc Natl Acad Sci U S A 96:1971–1976
Bapteste E, Boucher Y (2009) Epistemological impacts of horizontal gene transfer on classification in microbiology. In: Gogarten M, Gogarten J, Olendzenski L (eds) Horizontal gene transfer: genomes in flux, vol 532. Humana Press, New York
Bapteste E, O’Malley MA, Beiko RG, Ereshefsky M, Gogarten JP, Franklin-Hall L, Lapointe FJ, Dupré J, Dagan T, Boucher Y, Martin W (2009) Prokaryotic evolution and the tree of life are two different things. Biol Direct 4:34
Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102:14332–14337
Blankenship RE, Raymond J, Lince M, Larkum AWD, Jermiin LS, Lockhart PJ, Zhaxybayeva O, Gogarten JP (2001) Evolution of photosynthetic antennas and reaction centers. In: Proceedings of the 12th international congress on photosynthesis Melbourne, Australia, CSIRO Publishing, PL13
Boussau B, Gueguen L, Gouy M (2008) Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of Aquificales in the phylogeny of bacteria. BMC Evol Biol 8:272
Brochier C, Philippe H, Moreira D (2000) The evolutionary history of ribosomal protein RpS14: horizontal gene transfer at the heart of the ribosome. Trends Genet 16:529–533
Chan CX, Darling AE, Beiko RG, Ragan MA (2009) Are protein domains modules of lateral genetic transfer? PLoS One 4:e4524
Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287
Dagan T, Martin W (2007) Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution. Proc Natl Acad Sci U S A 104:870–875
Dagan T, Artzy-Randrup Y, Martin W (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Natl Acad Sci U S A 105:10039–10044
Daubin V, Gouy M, Perriere G (2002) A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history. Genome Res 12:1080–1090
Doolittle WF (2004) W. Ford Doolittle. Curr Biol 14:R176–R177
Doolittle WF (2009) The practice of classification and the theory of evolution, and what the demise of Charles Darwin’s tree of life hypothesis means for both of them. Philos Trans R Soc Lond B Biol Sci 364:2221–2228
Farahi K, Pusch GD, Overbeek R, Whitman WB (2004) Detection of lateral gene transfer events in the prokaryotic tRNA synthetases by the ratios of evolutionary distances method. J Mol Evol 58:615–631
Fournier GP, Gogarten JP (2008) Evolution of acetoclastic methanogenesis in Methanosarcina via horizontal gene transfer from cellulolytic Clostridia. J Bacteriol 190:1124–1127
Franklin-Hall L (2010) Trashing the tree: bad reasons and good reasons. Biol Philos (this issue) [details to follow]
Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3:722–732
Geach P (1967) Identity. Rev Metaphys 21:3–12
Gogarten JP (1995) The early evolution of cellular life. Trends Ecol Evol 10:147–151
Gogarten JP, Hilario E (2006) Inteins, introns, and homing endonucleases: recent revelations about the life cycle of parasitic genetic elements. BMC Evol Biol 6:94
Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679–687
Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238
Gray GS, Fitch WM (1983) Evolution of antibiotic resistance genes: the DNA sequence of a kanamycin resistance gene from Staphylococcus aureus. Mol Biol Evol 1:57–66
Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana
Hilario E, Gogarten JP (1993) Horizontal transfer of ATPase genes—the tree of life becomes a net of life. Biosystems 31:111–119
House CH (2009) The tree of life viewed through the contents of genomes. Methods Mol Biol 532:141–161
Huang J, Gogarten JP (2006) Ancient horizontal gene transfer can benefit phylogenetic reconstruction. Trends Genet 22:361–366
Huang J, Gogarten JP (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8:R99
Huang J, Gogarten JP (2008) Concerted gene recruitment in early plant evolution. Genome Biol 9:R109
Huang J, Gogarten JP (2009) Ancient gene transfer as a tool in phylogenetic reconstruction. Methods Mol Biol 532:127–139
Huang J, Xu Y, Gogarten JP (2005) The presence of a haloarchaeal type tyrosyl-tRNA synthetase marks the opisthokonts as monophyletic. Mol Biol Evol 22:2142–2146
Hyde D (2008) Sorites Paradox http://plato.stanford.edu/archives/fall2008/entries/sorites-paradox/. In: Zalta EN (ed) The Stanford encyclopedia of philosophy (Fall 2008 Edition)
Igarashi N, Harada J, Nagashima S, Matsuura K, Shimada K, Nagashima KVP (2001) Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria. J Mol Evol 52:333
Jain R, Rivera MC, Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 96:3801–3806
Koonin EV, Wolf YI (2009) The fundamental units, processes and patterns of evolution, and the tree of life conundrum. Biol Direct 4:33
Lawrence JG, Hendrickson H (2005) Genome evolution in bacteria: order beneath chaos. Curr Opin Microbiol 8:572–578
Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404
Margulis L (2009) Genome acquisition in horizontal gene transfer: symbiogenesis and macromolecular sequence analysis. Methods Mol Biol 532:181–191
Margulis L, Sagan D (2002) Acquiring genomes: a theory of the origin of species. Basic Books, New York
Martin W, Brinkmann H, Savonna C, Cerff R (1993) Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci U S A 90:8692–8696
McCann A, Cotton JA, McInerney JO (2008) The tree of genomes: an empirical comparison of genome-phylogeny reconstruction methods. BMC Evol Biol 8:312
Miller SR, Augustine S, Olson TL, Blankenship RE, Selker J, Wood AM (2005) Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc Natl Acad Sci U S A 102:850–855
Mongodin EF, Nelson KE, Daugherty S, Deboy RT, Wister J, Khouri H, Weidman J, Walsh DA, Papke RT, Sanchez Perez G, Sharma AK, Nesbo CL, MacLeod D, Bapteste E, Doolittle WF, Charlebois RL, Legault B, Rodriguez-Valera F (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci U S A 102:18147–18152
Morandi A, Zhaxybayeva O, Gogarten JP, Graf J (2005) Evolutionary and diagnostic implications of intragenomic heterogeneity in the 16S rRNA gene in Aeromonas strains. J Bacteriol 187:6561–6564
O’Malley MA, Dupré J (2007) Size doesn’t matter: towards a more inclusive philosophy of biology. Biol Philos 22:155–191
Olendzenski L, Gogarten JP (2009) Gene transfer: who benefits? Methods Mol Biol 532:3–9
Olendzenski L, Liu L, Zhaxybayeva O, Murphey R, Shin DG, Gogarten JP (2000) Horizontal transfer of archaeal genes into the Deinococcaceae: detection by molecular and computer-based approaches. J Mol Evol 51:587–599
Olendzenski L, Zhaxybayeva O, Gogarten J (2001) What’s in a tree? Does horizontal gene transfer determine microbial taxonomy? In: Seckbach J (ed) Cellular origin and life in extreme habitats, vol 4. Kluwer, Dordrecht, pp 67–78
Olendzenski L, Zhaxybayeva O, Gogarten JP (2002) Horizontal gene transfer: a new taxonomic principle? In: Syvanen M, Kado CI (eds) Horizontal gene transfer. Academic Press, New York, pp 427–435
Papke RT (2009) A critique of prokaryotic species concepts. Methods Mol Biol 532:379–395
Plutarch (75) Theseus, translated by John Dryden. The Internet Classics Archive. Retrieved 7 Oct 2009
Puigbò P, Wolf YI, Koonin EV (2009) Search for a ‘tree of life’ in the thicket of the phylogenetic forest. J Biol 8:59
Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538
Schouls LM, Schot CS, Jacobs JA (2003) Horizontal transfer of segments of the 16S rRNA genes between species of the Streptococcus anginosus group. J Bacteriol 185:7241–7246
Sheppard SK, McCarthy ND, Falush D, Maiden MC (2008) Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237–239
Sorek R, Zhu Y, Creevey CJ, Francino MP, Bork P, Rubin EM (2007) Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318:1449–1452
Stoltzfus A (1999) On the possibility of constructive neutral evolution. J Mol Evol 49:169–181
Swithers KS, Gogarten JP, Fournier GP (2009) Trees in the web of life. J Biol 8:54
Wang Y, Zhang Z (2000) Comparative sequence analyses reveal frequent occurrence of short segments containing an abnormally high number of non-random base variations in bacterial rRNA genes. Microbiology 146:2845–2854
Wang Y, Zhang Z, Ramanan N (1997) The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes. J Bacteriol 179:3270–3276
Wolf YI, Rogozin IB, Grishin NV, Koonin EV (2002) Genome trees and the tree of life. Trends Genet 18:472–479
Yap WH, Zhang Z, Wang Y (1999) Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J Bacteriol 181:5201–5209
Zhaxybayeva O, Gogarten JP (2004) Cladogenesis, coalescence and the evolution of the three domains of life. Trends Genet 20:182–187
Zhaxybayeva O, Lapierre P, Gogarten JP (2004) Genome mosaicism and organismal lineages. Trends Genet 20:254–260
Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16:1099–1108
Zhaxybayeva O, Nesbo C, Doolittle WF (2007) Systematic overestimation of gene gain through false diagnosis of gene absence. Genome Biol 8:402
Zhaxybayeva O, Doolittle WF, Papke RT, Gogarten JP (2009a) Intertwined evolutionary histories of marine Synechococcus and Prochlorococcus marinus. Genome Biol Evol 1:325–339
Zhaxybayeva O, Swithers K, Lapierre P, Fournier G, Bickhart D, DeBoy R, Nelson K, Nesbo C, Doolittle W, Gogarten J, Noll K (2009b) On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proc Natl Acad Sci USA 106:5865–5870
Acknowledgments
We thank the National Science Foundation Assembling the Tree of Life program (DEB 0830024) for support. This paper was first presented at the workshop, Perspectives on the Tree of Life, sponsored by the Leverhulme Trust and held in Halifax, Nova Scotia, July, 2009.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Andam, C.P., Williams, D. & Gogarten, J.P. Natural taxonomy in light of horizontal gene transfer. Biol Philos 25, 589–602 (2010). https://doi.org/10.1007/s10539-010-9212-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10539-010-9212-8