Abstract
Three quarters of the eukaryotic genes that can be traced back to prokaryotes are of bacterial origin, although eukaryotes evolved from the archaeal domain. This observation has inspired a multitude of hypotheses for the origin of the eukaryotic cell, including various fusion and endosymbiotic events. In this chapter, I argue that gene transfer between bacteria and eukaryotes over a long evolutionary time is sufficient to explain the observations of the mixed ancestry of eukaryotic genes. Lateral gene transfer is an evolutionary mechanism that steadily gains acceptance also in eukaryotic genomics. Recent data indeed suggest that most eukaryotic lineages are affected by gene transfer, that the process is ongoing, and that the fraction of genes affected probably is underestimated in most genome-wide analyses. Furthermore, studies of photosynthetic eukaryotes show that lateral gene transfer often operates in parallel with endosymbiotic gene transfer in organisms with secondary plastids. A similar mixture of influx of genes from both the endosymbionts and diverse external sources probably also occurred in the primary endosymbiotic events, which would explain the large amount of bacterial genes in the eukaryotic nucleus.
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References
Brown JR, Doolittle WF (1997) Archaea and the prokaryote-to-eukaryote transition. Microbiol Mol Biol Rev 61:456–502
Feng DF, Cho G, Doolittle RF (1997) Determining divergence times with a protein clock: update and reevaluation. Proc Natl Acad Sci U S A 94:13028–13033
Gupta RS (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62:1435–1491
Ribeiro S, Golding GB (1998) The mosaic nature of the eukaryotic nucleus. Mol Biol Evol 15:779–788
Esser C, Ahmadinejad N, Wiegand C et al (2004) A genome phylogeny for mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol 21:1643–1660
Cotton JA, McInerney JO (2010) Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function. Proc Natl Acad Sci U S A 107:17252–17255
Cox CJ, Foster PG, Hirt RP et al (2008) The archaebacterial origin of eukaryotes. Proc Natl Acad Sci U S A 105:20356–20361
Guy L, Ettema TJ (2011) The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol 19:580–587
Lake JA, Henderson E, Oakes M et al (1984) Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc Natl Acad Sci U S A 81:3786–3790
Hartman H, Fedorov A (2002) The origin of the eukaryotic cell: a genomic investigation. Proc Natl Acad Sci U S A 99:1420–1425
Gupta RS, Golding GB (1996) The origin of the eukaryotic cell. Trends Biochem Sci 21:166–171
Horiike T, Hamada K, Kanaya S et al (2001) Origin of eukaryotic cell nuclei by symbiosis of Archaea in Bacteria is revealed by homology-hit analysis. Nat Cell Biol 3:210–214
Rivera MC, Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152–155
Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311
Richards TA (2011) Genome evolution: horizontal movements in the fungi. Curr Biol:21:R166–R168
Dunning Hotopp JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27:157–163
Andersson JO (2009) Gene transfer and diversification of microbial eukaryotes. Annu Rev Microbiol 63:177–193
Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618
Archibald JM, Rogers MB, Toop M et al (2003) Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci U S A 100:7678–7683
Moustafa A, Beszteri B, Maier UG et al (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726
Chan CX, Reyes-Prieto A, Bhattacharya D (2011) Red and green algal origin of diatom membrane transporters: insights into environmental adaptation and cell evolution. PLoS ONE 6:e29138
Maruyama S, Suzaki T, Weber AP et al (2011) Eukaryote-to-eukaryote gene transfer gives rise to genome mosaicism in euglenids. BMC Evol Biol 11:105
Woehle C, Dagan T, Martin WF et al (2011) Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and apicomplexa-related Chromera velia. Genome Biol Evol 3:1220–1230
Burki F, Flegontov P, Obornik M et al (2012) Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genome Biol Evol 4:626–635
Deschamps P, Moreira D (2012) Reevaluating the green contribution to diatom genomes. Genome Biol Evol 4:683–688
Jerlström-Hultqvist J, Franzén O, Ankarklev J et al (2010) Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 11:543
Franzén O, Jerlström-Hultqvist J, Castro E et al (2009) Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: are human giardiasis caused by two different species? PLoS Pathog 5(8):e1000560
Pombert JF, Selman M, Burki F et al (2012) Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proc Natl Acad Sci U S A 109:12638–12643
Acuna R, Padilla BE, Florez-Ramos CP et al (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci U S A 109:4197–4202
Friesen TL, Stukenbrock EH, Liu Z et al (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38:953–956
Corradi N, Pombert JF, Farinelli L et al (2010) The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat Commun 1:77
Selman M, Pombert JF, Solter L et al (2011) Acquisition of an animal gene by microsporidian intracellular parasites. Curr Biol 21:R576–R577
Oliver RP, Solomon PS (2008) Recent fungal diseases of crop plants: is lateral gene transfer a common theme? Mol Plant-Microbe Interact 21:287–293
Andersson JO, Sjögren ÅM, Davis LAM et al (2003) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13:94–104
Morrison HG, McArthur AG, Gillin FD et al (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921–1926
Loftus B, Anderson I, Davies R et al (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433:865–868
Carlton JM, Hirt RP, Silva JC et al (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207–212
Bowler C, Allen AE, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244
Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62:1182–1197
Salzberg SL, White O, Peterson J et al (2001) Microbial genes in the human genome: lateral transfer or gene loss? Science 292:1903–1906
Ni T, Yue J, Sun G et al (2012) Ancient gene transfer from algae to animals: mechanisms and evolutionary significance. BMC Evol Biol 12:83
Gladyshev EA, Meselson M, Arkhipova IR (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320:1210–1213
Danchin EG, Rosso MN, Vieira P et al (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci U S A 107:17651–17656
Mayer WE, Schuster LN, Bartelmes G et al (2011) Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC Evol Biol 11:13
Dieterich C, Sommer RJ (2009) How to become a parasite—lessons from the genomes of nematodes. Trends Genet 25:203–209
Strope PK, Nickerson KW, Harris SD et al (2011) Molecular evolution of urea amidolyase and urea carboxylase in fungi. BMC Evol Biol 11:80
Slot JC, Rokas A (2011) Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol 21:134–139
Fitzpatrick DA (2012) Horizontal gene transfer in fungi. FEMS Microbiol Lett 329:1–8
Lawrence DP, Kroken S, Pryor BM et al (2011) Interkingdom gene transfer of a hybrid NPS/PKS from Bacteria to filamentous Ascomycota. PLoS ONE 6:e28231
Yue J, Hu X, Sun H et al (2012) Widespread impact of horizontal gene transfer on plant colonization of land. Nat Commun 3:1152
Fritz-Laylin LK, Prochnik SE, Ginger ML et al (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140:631–642
Eichinger L, Pachebat JA, Glöckner G et al (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57
Andersson JO (2011) Evolution of patchily distributed proteins shared between eukaryotes and prokaryotes: Dictyostelium as a case study. J Mol Microbiol Biotechnol 20:83–95
Andersson JO (2012) Phylogenomic approaches underestimate eukaryotic gene transfer. Mob Genet Elements 2:1–4
Moran Y, Fredman D, Szczesny P et al (2012) Recurrent horizontal transfer of bacterial toxin genes to eukaryotes. Mol Biol Evol 29:2223–2230
McDonald TR, Dietrich FS, Lutzoni F (2011) Multiple horizontal gene transfers of ammonium transporters/ammonia permeases from prokaryotes to eukaryotes: toward a new functional and evolutionary classification. Mol Biol Evol 29:51–60
Nosenko T, Bhattacharya D (2007) Horizontal gene transfer in chromalveolates. BMC Evol Biol 7:173
Andersson JO, Sjögren ÅM, Horner DS et al (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
Richards TA, Soanes DM, Jones MD et al (2011) Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci U S A 108:15258–15263
Hug LA, Stechmann A, Roger AJ (2010) Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol Biol Evol 27:311–324
Stairs CW, Roger AJ, Hampl V (2011) Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a Firmicute. Mol Biol Evol 28:2087–2099
Hampl V, Stairs CV, Roger AJ (2011) The tangled past of eukaryotic enzymes involved in anaerobic metabolism. Mob Genet Elements 1:71–74
Huang J, Gogarten JP (2006) Ancient horizontal gene transfer can benefit phylogenetic reconstruction. Trends Genet 22:361–366
Nowack EC, Melkonian M, Glockner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18:410–418
Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:R81–R88
Fast NM, Kissinger JC, Roos DS et al (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18:418–426
Andersson JO, Roger AJ (2002) A cyanobacterial gene in nonphotosynthetic protists—an early chloroplast acquisition in eukaryotes? Curr Biol 12:115–119
Roger AJ, Svärd SG, Tovar J et al (1998) A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci U S A 95:229–234
Maruyama S, Matsuzaki M, Misawa K et al (2009) Cyanobacterial contribution to the genomes of the plastid-lacking protists. BMC Evol Biol 9:197
Reyes-Prieto A, Moustafa A, Bhattacharya D (2008) Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr Biol 18:956–962
Tyler BM, Tripathy S, Zhang X et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266
Sun G, Yang Z, Ishwar A et al (2010) Algal genes in the closest relatives of animals. Mol Biol Evol 27:2879–2889
Stiller JW, Huang J, Ding Q et al (2009) Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genomics 10:484
Dagan T, Martin W (2009) Microbiology. Seeing green and red in diatom genomes. Science 324:1651–1652
Huang J, Gogarten JP (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8:R99
Becker B, Hoef-Emden K, Melkonian M (2008) Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol Biol 8:203
McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21:1366–1372
von Dohlen CD, Kohler S, Alsop ST et al (2001) Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412:433–436
Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102:14332–14337
Nelson KE, Clayton RA, Gill SR et al (1999) Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329
Johny S, Larson TM, Solter LF et al (2009) Phylogenetic characterization of Encephalitozoon romaleae (Microsporidia) from a grasshopper host: relationship to Encephalitozoon spp. infecting humans. Infect Genet Evol 9:189–195
Parfrey LW, Grant J, Tekle YI et al (2010) Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Syst Biol 59:518–533
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Andersson, J. (2013). Gene Transfer and the Chimeric Nature of Eukaryotic Genomes. In: Gophna, U. (eds) Lateral Gene Transfer in Evolution. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7780-8_10
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