Horizontal Acquisition of Prokaryotic Genes for Eukaryote Functioning and Niche Adaptation

  • Maxime Bruto
  • Claire Prigent-Combaret
  • Patricia Luis
  • Grégory Hoff
  • Yvan Moënne-Loccoz
  • Daniel Muller


Horizontal gene transfer (HGT) is a major mechanism of evolution, in that it is pervasive and can dramatically affect lifestyle by allowing adaptation to specialized niches. Although research has mostly focused on HGT within prokaryotes, examples of inter-domain transfers from prokaryotes to eukaryotes are increasing, and such inter-domain HGT is emerging as a very significant component in ecological and evolutionary terms. Here, different cases of intra- and inter-domain HGT conferring an adaptive advantage to eukaryotes are reviewed to examine novel trends and HGT paradigms. Thus, HGT appears to play an important role in eukaryotic adaptation to specific environmental conditions, including in the ecological evolution toward parasitic lifestyles and pathogenesis. The diversity of prokaryotes and their genetic potential are emerging as a vast reservoir to foster rapid eukaryote evolution.


Lateral gene transfer (LGT) Interdomain gene transfer HGT dynamic 


  1. Abby SS, Tannier E, Gouy M, Daubin V (2012) Lateral gene transfer as a support for the tree of life. Proc Natl Acad Sci USA 109:4962–4967PubMedCrossRefGoogle Scholar
  2. Acuña R, Padilla BE, Flórez-Ramos CP, Rubio JD, Herrera JC, Benavides P, Lee S-J, Yeats TH, Egan AN, Doyle JJ et al (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci USA 109:4197–4202PubMedGoogle Scholar
  3. Akagi Y, Akamatsu H, Otani H, Kodama M (2009) Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8:1732–1738PubMedCrossRefGoogle Scholar
  4. Anderson MT, Seifert HS (2011) Opportunity and means: horizontal gene transfer from the human host to a bacterial pathogen. MBio 2:e00005–e00011PubMedCrossRefGoogle Scholar
  5. Andersson JO (2009) Gene transfer and diversification of microbial eukaryotes. Annu Rev Microbiol 63:177–193PubMedCrossRefGoogle Scholar
  6. Aoki S, Syōno K (1999) Horizontal gene transfer and mutation: Ngrol genes in the genome of Nicotiana glauca. Proc Natl Acad Sci USA 96:13229–13234PubMedCrossRefGoogle Scholar
  7. Archibald J, Rogers M, Toop M, Ishida K, Keeling P (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
  8. Arsène-Ploetze F, Koechler S, Marchal M, Coppée J-Y, Chandler M et al (2010) Structure, function, and evolution of the Thiomonas spp. genome. PLoS Genet 6:e1000859PubMedCrossRefGoogle Scholar
  9. Belbahri L, Calmin G, Mauch F, Andersson JO (2008) Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 408:1–8PubMedCrossRefGoogle Scholar
  10. Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201PubMedCrossRefGoogle Scholar
  11. Bergthorsson U, Richardson A, Young G, Goertzen L, Palmer J (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA 101:17747–17752PubMedCrossRefGoogle Scholar
  12. Bock R (2010) The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15:11–22PubMedCrossRefGoogle Scholar
  13. Boschetti C, Carr A, Crisp A, Eyres I, Wang-Koh Y, Lubzens E, Barraclough TG, Micklem G, Tunnacliffe A (2012) Biochemical diversification through foreign gene expression in bdelloid rotifers. PLoS Genet 8:e1003035PubMedCrossRefGoogle Scholar
  14. Boto L (2010) Horizontal gene transfer in evolution: facts and challenges. Proc R Soc B 277:819–827PubMedCrossRefGoogle Scholar
  15. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D et al (2010) The dynamic genome of Hydra. Nature 464:592–596PubMedCrossRefGoogle Scholar
  16. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, Grimwood J, Schmutz J, Taga M, White GJ, Zhou S et al (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5:e1000618PubMedCrossRefGoogle Scholar
  17. Cook RJ, Thomashow LS, Weller DM, Fujimoto D, Mazzola M, Bangera G, Kim D (1995) Molecular mechanisms of defense by rhizobacteria against root disease. Proc Natl Acad Sci USA 92:4197–4201PubMedCrossRefGoogle Scholar
  18. Dagan T, Artzy-Randrup Y, Martin W (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Natl Acad Sci USA 105:10039–10044PubMedCrossRefGoogle Scholar
  19. Danchin EG (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 107:17651–17656PubMedCrossRefGoogle Scholar
  20. Danchin EG (2011) What nematode genomes tell us about the importance of horizontal gene transfers in the evolutionary history of animals. Mob Genet Elem 1: 269–292Google Scholar
  21. Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990) Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124:339–355PubMedGoogle Scholar
  22. de la Cruz F, Davies J (2000) Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol 8:128–133PubMedCrossRefGoogle Scholar
  23. Doolittle W (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
  24. Dubey GP, Ben-Yehuda S (2011) Intercellular nanotubes mediate bacterial communication. Cell 144:590–600PubMedCrossRefGoogle Scholar
  25. Dunning Hotopp JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27:157–163PubMedCrossRefGoogle Scholar
  26. Dunning Hotopp JC, Clark ME, Oliveira DCSG, Foster JM, Fischer P, Muñoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S et al (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756PubMedCrossRefGoogle Scholar
  27. Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78:737–756PubMedGoogle Scholar
  28. Fenn K, Conlon C, Jones M, Quail MA, Holroyd NE, Parkhill J, Blaxter M (2006) Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2:e94PubMedCrossRefGoogle Scholar
  29. Filée J, Siguier P, Chandler M (2007) I am what I eat and I eat what I am: acquisition of bacterial genes by giant viruses. Trends Genet 23:10–15PubMedCrossRefGoogle Scholar
  30. Frapolli M, Pothier JF, Défago G, Moënne-Loccoz Y (2012) Evolutionary history of synthesis pathway genes for phloroglucinol and cyanide antimicrobials in plant-associated fluorescent pseudomonads. Mol Phylogenet Evol 63:877–890PubMedCrossRefGoogle Scholar
  31. Garcia-Vallvé S, Romeu A, Palau J (2000) Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol 17:352–361PubMedCrossRefGoogle Scholar
  32. Gladyshev EA, Meselson M, Arkhipova IR (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320:1210–1213PubMedCrossRefGoogle Scholar
  33. Graham LA, Lougheed SC, Ewart KV, Davies PL (2008) Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS ONE 3:e2616PubMedCrossRefGoogle Scholar
  34. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Thi Ngoc PC, Ortego F et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487–492PubMedCrossRefGoogle Scholar
  35. Haegeman A, Jones JT, Danchin EGJ (2011) Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Mol Plant-Microbe Interact 24:879–887PubMedCrossRefGoogle Scholar
  36. Hall C, Brachat S, Dietrich FS (2005) Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot Cell 4:1102–1115PubMedCrossRefGoogle Scholar
  37. Hughes AL, Friedman R (2005) Poxvirus genome evolution by gene gain and loss. Mol Phylogenet Evol 35:186–195PubMedCrossRefGoogle Scholar
  38. Hughes AL, Irausquin S, Friedman R (2010) The evolutionary biology of poxviruses. Infect Genet Evol 10:50–59PubMedCrossRefGoogle Scholar
  39. Jackson D, Macis L, Reitner J, Worheide G (2011) A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy. BMC Evol Biol 11:238PubMedCrossRefGoogle Scholar
  40. Keeling P, Palmer J (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618PubMedCrossRefGoogle Scholar
  41. Keeling PJ (2009) Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr Opin Genet Dev 19:613–619PubMedCrossRefGoogle Scholar
  42. Keeling PJ, Inagaki Y (2004) A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1alpha. Proc Natl Acad Sci USA 101:15380–15385PubMedCrossRefGoogle Scholar
  43. Kidarsa TA, Goebel NC, Zabriskie TM, Loper JE (2011) Phloroglucinol mediates cross-talk between the pyoluteorin and 2,4-diacetylphloroglucinol biosynthetic pathways in Pseudomonas fluorescens Pf-5. Mol Microbiol 81:395–414PubMedCrossRefGoogle Scholar
  44. Klotz MG, Loewen PC (2003) The molecular evolution of catalatic hydroperoxidases: evidence for multiple lateral transfer of genes between prokaryota and from bacteria into eukaryota. Mol Biol Evol 20:1098–1112PubMedCrossRefGoogle Scholar
  45. Koonin E (2009) Darwinian evolution in the light of genomics. Nucleic Acids Res 37:1011–1034PubMedCrossRefGoogle Scholar
  46. Koonin E, Makarova K, Aravind L (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55:709–742PubMedCrossRefGoogle Scholar
  47. Koonin E, Wolf Y (2009) Is evolution Darwinian or/and Lamarckian? Biol Direct 4:42PubMedCrossRefGoogle Scholar
  48. Kunik T, Tzfira T, Kapulnik Y, Gafni Y, Dingwall C, Citovsky V (2001) Genetic transformation of HeLa cells by Agrobacterium. Proc Natl Acad Sci USA 98:1871–1876PubMedCrossRefGoogle Scholar
  49. Kunin V, Ouzounis CA (2003) The balance of driving forces during genome evolution in prokaryotes. Genome Res 13:1589–1594PubMedCrossRefGoogle Scholar
  50. Kuo C-H, Ochman H (2009) The fate of new bacterial genes. FEMS Microbiol Rev 33:38–43PubMedCrossRefGoogle Scholar
  51. Lander ES (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedCrossRefGoogle Scholar
  52. Lang A, Beatty J (2007) Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends Microbiol 15:54–62PubMedCrossRefGoogle Scholar
  53. Lassalle F, Campillo T, Vial L, Baude J, Costechareyre D, Chapulliot D, Shams M, Abrouk D, Lavire C, Oger-Desfeux C et al (2011) Genomic species are ecological species as revealed by comparative genomics in Agrobacterium tumefaciens. Genome Biol Evol 3:762–781PubMedCrossRefGoogle Scholar
  54. Lawrence JG, Ochman H (1997) Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44:383–397PubMedCrossRefGoogle Scholar
  55. Lerat E, Daubin V, Ochman H, Moran NA (2005) Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3:e130PubMedCrossRefGoogle Scholar
  56. Li Z-W, Shen Y-H, Xiang Z-H, Zhang Z (2011) Pathogen-origin horizontally transferred genes contribute to the evolution of Lepidopteran insects. BMC Evol Biol 11:356PubMedCrossRefGoogle Scholar
  57. Lurie-Weinberger MN, Gomez-Valero L, Merault N, Glöckner G, Buchrieser C, Gophna U (2010) The origins of eukaryotic-like proteins in Legionella pneumophila. Int J Med Microbiol 300:470–481PubMedCrossRefGoogle Scholar
  58. Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B et al (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373PubMedCrossRefGoogle Scholar
  59. Marcet-Houben M, Gabaldón T (2010) Acquisition of prokaryotic genes by fungal genomes. Trends Genet 26:5–8PubMedCrossRefGoogle Scholar
  60. Matveeva TV, Bogomaz DI, Pavlova OA, Nester EW, Lutova LA (2012) Horizontal gene transfer from genus Agrobacterium to the plant Linaria in Nature. Mol Plant-Microbe Interact 25:1542–1551PubMedCrossRefGoogle Scholar
  61. Moran Y, Fredman D, Szczesny P, Grynberg M, Technau U (2012) Recurrent horizontal transfer of bacterial toxin genes to eukaryotes. Mol Biol Evol 29:2223–2230PubMedCrossRefGoogle Scholar
  62. Muller D, Médigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsène-Ploetze F, Carapito C et al (2007) A tale of two oxidation states: bacterial colonization of arsenic-rich environments. PLoS Genet 3:e53PubMedCrossRefGoogle Scholar
  63. Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 106:2–9PubMedGoogle Scholar
  64. Nelson KE (1999) Evidence for lateral gene transfer between archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329PubMedCrossRefGoogle Scholar
  65. Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInerney JO, Deppenmeier U, Martin WF (2012) Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc Natl Acad Sci USA 109:20537–20542PubMedCrossRefGoogle Scholar
  66. Nikoh N, Hosokawa T, Oshima K, Hattori M, Fukatsu T (2011) Reductive evolution of bacterial genome in insect gut environment. Genome Biol Evol 3:702–714PubMedCrossRefGoogle Scholar
  67. Nikoh N, McCutcheon JP, Kudo T, Miyagishima SY, Moran NA, Nakabachi A (2010) Bacterial genes in the Aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 6:e1000827PubMedCrossRefGoogle Scholar
  68. Nikoh N, Tanaka K, Shibata F, Kondo N, Hizume M, Shimada M, Fukatsu T (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18:272–280PubMedCrossRefGoogle Scholar
  69. Ochman H, Lawrence J, Groisman E (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304PubMedCrossRefGoogle Scholar
  70. Ochman H, Moran NA (2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292:1096–1099PubMedCrossRefGoogle Scholar
  71. Patrick S, Blakely GW (2012) Crossing the eukaryote-prokaryote divide: a ubiquitin homolog in the human commensal bacterium Bacteroides fragilis. Mob Genet Elem 2:149–151CrossRefGoogle Scholar
  72. Popa O, Hazkani-Covo E, Landan G, Martin W, Dagan T (2011) Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. Genome Res 21:599–609PubMedCrossRefGoogle Scholar
  73. Pothier JF, Prigent-Combaret C, Haurat J, Moënne-Loccoz Y, Wisniewski-Dyé F (2008) Duplication of plasmid-borne nitrite reductase gene nirK in the wheat-associated plant growth-promoting rhizobacterium Azospirillum brasilense Sp245. Mol Plant-Microbe Interact 21:831–842PubMedCrossRefGoogle Scholar
  74. Prigent-Combaret C, Blaha D, Pothier J, Vial L, Poirier M, Wisniewski-Dyé F, Moënne-Loccoz Y (2008) Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. FEMS Microbiol Ecol 65:202–219PubMedCrossRefGoogle Scholar
  75. Puigbo P, Wolf Y, Koonin E (2009) Search for a tree of life in the thicket of the phylogenetic forest. J Biol 8:59PubMedCrossRefGoogle Scholar
  76. Ramette A, Moënne-Loccoz Y, Défago G (2001) Polymorphism of the polyketide synthase gene phlD in biocontrol fluorescent pseudomonads producing 2,4-diacetylphloroglucinol and comparison of PhlD with plant polyketide synthases. Mol Plant-Microbe Interact 14:639–652PubMedCrossRefGoogle Scholar
  77. Raz Y, Tannenbaum E (2010) The influence of horizontal gene transfer on the mean fitness of unicellular populations in static environments. Genetics 185:327–337PubMedCrossRefGoogle Scholar
  78. Redrejo-Rodríguez M, Muñoz-Espín D, Holguera I, Mencía M, Salas M (2012) Functional eukaryotic nuclear localization signals are widespread in terminal proteins of bacteriophages. Proc Natl Acad Sci USA 109:18482–18487PubMedCrossRefGoogle Scholar
  79. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ (2009) Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. The Plant Cell Online 21: 1897–1911Google Scholar
  80. Richards TA, Soanes DM, Jones MDM, Vasieva O, Leonard G, Paszkiewicz K, Foster PG, Hall N, Talbot NJ (2011) Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci USA 108:15258–15263PubMedCrossRefGoogle Scholar
  81. Rogers MB (2007) A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evol Biol 7:89PubMedCrossRefGoogle Scholar
  82. Sagane Y, Zech K, Bouquet J-M, Schmid M, Bal U, Thompson EM (2010) Functional specialization of cellulose synthase genes of prokaryotic origin in chordate larvaceans. Development 137:1483–1492PubMedCrossRefGoogle Scholar
  83. 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
  84. Sanders IR (2006) Rapid disease emergence through horizontal gene transfer between eukaryotes. Trends Ecol Evol 21:656–658PubMedCrossRefGoogle Scholar
  85. Scholl E, Thorne J, McCarter J, Bird DM (2003) Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4:R39PubMedCrossRefGoogle Scholar
  86. Schröder G, Schuelein R, Quebatte M, Dehio C (2011) Conjugative DNA transfer into human cells by the VirB/VirD4 type IV secretion system of the bacterial pathogen Bartonella henselae. Proc Natl Acad Sci USA 108:14643–14648PubMedCrossRefGoogle Scholar
  87. Slot JC, Rokas A (2011) Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between Fungi. Curr Biol 21:134–139PubMedCrossRefGoogle Scholar
  88. Sormacheva I, Smyshlyaev G, Mayorov V, Blinov A, Novikov A, Novikova O (2012) Vertical evolution and horizontal transfer of CR1 Non-LTR Retrotransposons and Tc1/mariner DNA transposons in Lepidoptera species. Mol Biol Evol 29:3685–3702PubMedCrossRefGoogle Scholar
  89. Stegemann S, Bock R (2009) Exchange of genetic material between cells in plant tissue grafts. Science 324:649–651PubMedCrossRefGoogle Scholar
  90. Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci USA 100:8828–8833PubMedCrossRefGoogle Scholar
  91. Sun BF, Xiao JH, He SM, Liu L, Murphy RW, Huang DW (2013) Multiple ancient horizontal gene transfers and duplications in lepidopteran species. Insect Mol Biol 22:72–87PubMedCrossRefGoogle Scholar
  92. Syvanen M (2012) Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46:341–358PubMedCrossRefGoogle Scholar
  93. Treangen TJ, Rocha EPC (2011) Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7:e1001284PubMedCrossRefGoogle Scholar
  94. Vial L, Lavire C, Mavingui P, Blaha D, Haurat J, Moënne-Loccoz Y, Bally R, Wisniewski-Dyé F (2006) Phase variation and genomic architecture changes in Azospirillum. J Bacteriol 188:5364–5373PubMedCrossRefGoogle Scholar
  95. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, The Nasonia Genome Working Group (2010). Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343–348Google Scholar
  96. Werner S, Steiner U, Bechner R, Kortekamp A, Zyprian E, Deising HB (2002) Chitin synthesis during in planta growth and asexual propagation of the cellulosic oomycete and obligate biotrophic grapevine pathogen plasmopara viticola. FEMS Microbiol Letters 208: 169–173Google Scholar
  97. Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov LO, Wuichet K, Hurst GB, McDonald WH, Robertson JS, Barbe V et al (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7:e1002430PubMedCrossRefGoogle Scholar
  98. Wybouw N, Balabanidou V, Ballhorn DJ, Dermauw W, Grbić M, Vontas J, Van Leeuwen T (2012) A horizontally transferred cyanase gene in the spider mite Tetranychus urticae is involved in cyanate metabolism and is differentially expressed upon host plant change. Insect Biochem Mol Biol 42:881–889PubMedCrossRefGoogle Scholar
  99. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P et al (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5:e156PubMedCrossRefGoogle Scholar
  100. Yue J, Hu X, Sun H, Yang Y, Huang J (2012) Widespread impact of horizontal gene transfer on plant colonization of land. Nat Commun 3:1152PubMedCrossRefGoogle Scholar
  101. Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16:1099–1108PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Maxime Bruto
    • 1
    • 2
    • 3
  • Claire Prigent-Combaret
    • 1
    • 2
    • 3
  • Patricia Luis
    • 1
    • 2
    • 3
  • Grégory Hoff
    • 1
    • 2
    • 3
  • Yvan Moënne-Loccoz
    • 1
    • 2
    • 3
  • Daniel Muller
    • 1
    • 2
    • 3
  1. 1.Université de LyonLyonFrance
  2. 2.Université Lyon 1VilleurbanneFrance
  3. 3.CNRSUMR5557, Ecologie MicrobienneVilleurbanneFrance

Personalised recommendations