, Volume 17, Issue 4, pp 545–563 | Cite as

How hyperthermophiles adapt to change their lives: DNA exchange in extreme conditions

  • Marleen van Wolferen
  • Małgorzata Ajon
  • Arnold J. M. Driessen
  • Sonja-Verena Albers


Transfer of DNA has been shown to be involved in genome evolution. In particular with respect to the adaptation of bacterial species to high temperatures, DNA transfer between the domains of bacteria and archaea seems to have played a major role. In addition, DNA exchange between similar species likely plays a role in repair of DNA via homologous recombination, a process that is crucial under DNA damaging conditions such as high temperatures. Several mechanisms for the transfer of DNA have been described in prokaryotes, emphasizing its general importance. However, until recently, not much was known about this process in prokaryotes growing in highly thermophilic environments. This review describes the different mechanisms of DNA transfer in hyperthermophiles, and how this may contribute to the survival and adaptation of hyperthermophilic archaea and bacteria to extreme environments.


Thermophiles DNA transfer Adaptation Conjugation 



M.vW was supported by a grant from the German Science Foundation (DFG, AL1206/3-1). M.A was supported by an ALW grant from the Dutch Science Organization (NWO). S.V.A. received support from intramural funds of the Max Planck Society.


  1. Aagaard C, Dalgaard JZ, Garrett RA (1995) Intercellular mobility and homing of an archaeal rDNA intron confers a selective advantage over intron- cells of Sulfolobus acidocaldarius. Proc Natl Acad Sci USA 92:12285–12289PubMedCrossRefGoogle Scholar
  2. Ackermann HW (1996) Frequency of morphological phage descriptions in 1995. Arch Virol 141:209–218PubMedCrossRefGoogle Scholar
  3. Ackermann HW (2001) Frequency of morphological phage descriptions in the year 2000. Brief review. Arch Virol 146:843–857PubMedCrossRefGoogle Scholar
  4. Ackermann HW (2007) 5500 Phages examined in the electron microscope. Arch Virol 152:227–243PubMedCrossRefGoogle Scholar
  5. Ackermann HW, Prangishvili D (2012) Prokaryote viruses studied by electron microscopy. Arch Virol 157:1843–1849PubMedCrossRefGoogle Scholar
  6. Ajon M, Fröls S, van Wolferen M et al (2011) UV-inducible DNA exchange in hyperthermophilic archaea mediated by type IV pili. Mol Microbiol 82:807–817PubMedCrossRefGoogle Scholar
  7. Alvarez L, Bricio C, Gómez MJ, Berenguer J (2011) Lateral transfer of the denitrification pathway genes among Thermus thermophilus strains. Appl Environ Microbiol 77:1352–1358PubMedCrossRefGoogle Scholar
  8. Alvarez-Martinez CE, Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73:775–808PubMedCrossRefGoogle Scholar
  9. Anderson AW, Nordon HC, Cain RF et al (1956) Studies on a radio-resistant micrococcus. I. Isolation, morphology, cultural characteristics, and resistance to gamma radiation. Food Technol 10:575–578Google Scholar
  10. Aravind L, Tatusov RL, Wolf YI et al (1998) Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet 14:442–444PubMedCrossRefGoogle Scholar
  11. Arnold HP, She Q, Phan H et al (1999) The genetic element pSSVx of the extremely thermophilic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol Microbiol 34:217–226PubMedCrossRefGoogle Scholar
  12. Assalkhou R, Balasingham S, Collins RF et al (2007) The outer membrane secretin PilQ from Neisseria meningitidis binds DNA. Microbiology 153:1593–1603PubMedCrossRefGoogle Scholar
  13. Atomi H, Matsumi R, Imanaka T (2004) Reverse gyrase is not a prerequisite for hyperthermophilic life. J Bacteriol 186:4829–4833PubMedCrossRefGoogle Scholar
  14. Averhoff B (2009) Shuffling genes around in hot environments: the unique DNA transporter of Thermus thermophilus. FEMS Microbiol Rev 33:611–626PubMedCrossRefGoogle Scholar
  15. Averhoff B, Friedrich A (2003) Type IV pili-related natural transformation systems: DNA transport in mesophilic and thermophilic bacteria. Arch Microbiol 180:385–393PubMedCrossRefGoogle Scholar
  16. Averhoff B, Müller V (2010) Exploring research frontiers in microbiology: recent advances in halophilic and thermophilic extremophiles. Res Microbiol 161:506–514PubMedCrossRefGoogle Scholar
  17. Ayora S, Carrasco B, Cárdenas PP et al (2011) Double-strand break repair in bacteria: a view from Bacillus subtilis. FEMS Microbiol Rev 35:1055–1081PubMedCrossRefGoogle Scholar
  18. Basen M, Sun J, Adams MWW (2012) Engineering a hyperthermophilic archaeon for temperature-dependent product formation. mBio 3:e00053–12Google Scholar
  19. Basta T, Smyth J, Forterre P et al (2009) Novel archaeal plasmid pAH1 and its interactions with the lipothrixvirus AFV1. Mol Microbiol 71:23–34PubMedCrossRefGoogle Scholar
  20. Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA 102:14332–14337PubMedCrossRefGoogle Scholar
  21. Bernstein H, Byers G, Michod R (1981) Evolution of sexual reproduction: importance of DNA repair, complementation, and variation. Am Nat 117:537–549CrossRefGoogle Scholar
  22. Bernstein H, Bernstein C, Michod RE (2012) DNA repair as the primary adaptive function of sex in bacteria and eukaryotes. In: Kimura S et al (eds) DNA repair: new research, Nova Science Publishers Inc, pp 1–49. ISBN: 978-1-62100-756-2Google Scholar
  23. Bertani G, Baresi L (1987) Genetic transformation in the methanogen Methanococcus voltae PS. J Bacteriol 169:2730–2738PubMedGoogle Scholar
  24. Bolduc B, Shaughnessy DP, Wolf YI et al (2012) Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J Virol 86:5562–5573PubMedCrossRefGoogle Scholar
  25. Bordenstein SR, Reznikoff WS (2005) Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3:688–699PubMedCrossRefGoogle Scholar
  26. Bricio C, Alvarez L, Gómez MJ, Berenguer J (2011) Partial and complete denitrification in Thermus thermophilus: lessons from genome drafts. Biochem Soc Trans 39:249–253PubMedCrossRefGoogle Scholar
  27. Brochier-Armanet C, Forterre P (2007) Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers. Archaea 2:83–93PubMedCrossRefGoogle Scholar
  28. Brock TD, Brock KM, Belly RT, Weiss RL (1972) Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol 84:54–68PubMedCrossRefGoogle Scholar
  29. Brüggemann H, Chen C (2006) Comparative genomics of Thermus thermophilus: plasticity of the megaplasmid and its contribution to a thermophilic lifestyle. J Bacteriol 124:654–661. doi: 10.1016/j.jbiotec.2006.03.043 Google Scholar
  30. Brüssow H, Canchaya C, Hardt W-D (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602PubMedCrossRefGoogle Scholar
  31. Burkhardt J, Vonck J, Averhoff B (2011) Structure and function of PilQ, a secretin of the DNA transporter from the thermophilic bacterium Thermus thermophilus HB27. J Biol Chem 286:9977–9984PubMedCrossRefGoogle Scholar
  32. Burkhardt J, Vonck J, Langer JD et al (2012) Unusual N-terminal ααβαββα fold of PilQ from Thermus thermophilus mediates ring formation and is essential for piliation. J Biol Chem 287:8484–8494PubMedCrossRefGoogle Scholar
  33. Cadillo-Quiroz H, Didelot X, Held NL et al (2012) Patterns of gene flow define species of thermophilic Archaea. PLoS Biol 10:e1001265PubMedCrossRefGoogle Scholar
  34. Campbell BJ, Smith JL, Hanson TE et al (2009) Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genet 5:e1000362PubMedCrossRefGoogle Scholar
  35. Canchaya C, Fournous G, Chibani-Chennoufi S et al (2003) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6:417–424PubMedCrossRefGoogle Scholar
  36. Capasso G, Favara R, Francofonte S, Inguaggiato S (1999) Chemical and isotopic variations in fumarolic discharge and thermal waters at Vulcano Island (Aeolian Islands, Italy) during 1996: evidence of resumed volcanic activity. J Volcanol Geoth Res 88:167–175CrossRefGoogle Scholar
  37. Ceballos RM, Marceau CD, Marceau JO et al (2012) Differential virus host-ranges of the Fuselloviridae of hyperthermophilic Archaea: implications for evolution in extreme environments. Front Microbiol 3:295PubMedCrossRefGoogle Scholar
  38. Cehovin A, Simpson PJ, McDowell MA et al (2013) Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci USA 110:3065–3070Google Scholar
  39. César CE, Álvarez L, Bricio C et al (2011) Unconventional lateral gene transfer in extreme thermophilic bacteria. Int Microbiol 14:187–199PubMedGoogle Scholar
  40. Charpentier X, Kay E, Schneider D, Shuman HA (2011) Antibiotics and UV radiation induce competence for natural transformation in Legionella pneumophila. J Bacteriol 193:1114–1121PubMedCrossRefGoogle Scholar
  41. Chen I, Dubnau D (2004) DNA uptake during bacterial transformation. Nat Rev Microbiol 2:241–249PubMedCrossRefGoogle Scholar
  42. Chen L, Brugger K, Skovgaard M et al (2005) The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187:4992–4999PubMedCrossRefGoogle Scholar
  43. Claverys J-P, Prudhomme M, Martin B (2006) Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu Rev Microbiol 60:451–475PubMedCrossRefGoogle Scholar
  44. Claverys J-P, Martin B, Polard P (2009) The genetic transformation machinery: composition, localization, and mechanism. FEMS Microbiol Rev 33:643–656PubMedCrossRefGoogle Scholar
  45. Cohan FM (1994a) Genetic exchange and evolutionary divergence in prokaryotes. Trends Ecol Evol 9:175–180PubMedCrossRefGoogle Scholar
  46. Cohan FM (1994b) The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes. Am Nat 143:965–986CrossRefGoogle Scholar
  47. Danner DB, Deich RA, Sisco KL, Smith HO (1980) An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene 11:311–318PubMedCrossRefGoogle Scholar
  48. Datta N, Kontomichalou P (1965) Penicillinase synthesis controlled by infectious R factors in Enterobacteriaceae. Nature 208:239–241PubMedCrossRefGoogle Scholar
  49. de la Cruz F, Frost LS, Meyer RJ, Zechner EL (2010) Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol Rev 34:18–40PubMedCrossRefGoogle Scholar
  50. Deatherage BL, Cookson BT (2012) Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 80:1948–1957PubMedCrossRefGoogle Scholar
  51. Déclais AC, Marsault J, Confalonieri F et al (2000) Reverse gyrase, the two domains intimately cooperate to promote positive supercoiling. J Biol Chem 275:19498–19504PubMedCrossRefGoogle Scholar
  52. Deich RA, Smith HO (1980) Mechanism of homospecific DNA uptake in Haemophilus influenzae transformation. Mol Gen Genet 177:369–374PubMedCrossRefGoogle Scholar
  53. Dickerson RE (1980) Evolution and gene transfer in purple photosynthetic bacteria. Nature 283:210–212PubMedCrossRefGoogle Scholar
  54. Diruggiero J, Dunn D, Maeder DL et al (2000) Evidence of recent lateral gene transfer among hyperthermophilic archaea. Mol Microbiol 38:684–693PubMedCrossRefGoogle Scholar
  55. Dorer MS, Fero J, Salama NR (2010) DNA damage triggers genetic exchange in Helicobacter pylori. PLoS Pathog 6:e1001026PubMedCrossRefGoogle Scholar
  56. Dorward DW, Garon CF, Judd RC (1989) Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J Bacteriol 171:2499–2505PubMedGoogle Scholar
  57. Drake JW (2009) Avoiding dangerous missense: thermophiles display especially low mutation rates. PLoS Genet 5:e1000520PubMedCrossRefGoogle Scholar
  58. Dubey GP, Ben-Yehuda S (2011) Intercellular nanotubes mediate bacterial communication. Cell 144:590–600PubMedCrossRefGoogle Scholar
  59. Dubnau D (1991) Genetic competence in Bacillus subtilis. Microbiol Rev 55:395–424PubMedGoogle Scholar
  60. Dubnau D (1999) DNA uptake in bacteria. Annu Rev Microbiol 53:217–244PubMedCrossRefGoogle Scholar
  61. Dykhuizen DE, Green L (1991) Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173:7257–7268PubMedGoogle Scholar
  62. Eisenstark A (1967) Bacteriophage techniques. In: Maramorosch K, Koprowski H (eds) Methods in virology, vol 1. Academic Press, NY, pp 449–525Google Scholar
  63. Elkins C, Thomas CE, Seifert HS, Sparling PF (1991) Species-specific uptake of DNA by gonococci is mediated by a 10-base-pair sequence. J Bacteriol 173:3911–3913PubMedGoogle Scholar
  64. Ellen AF, Albers S-V, Huibers W et al (2009) Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 13:67–79PubMedCrossRefGoogle Scholar
  65. Finkel SE, Kolter R (2001) DNA as a nutrient: novel role for bacterial competence gene homologs. J Bacteriol 183:6288–6293PubMedCrossRefGoogle Scholar
  66. Fitzmaurice WP, Benjamin RC, Huang PC, Scocca JJ (1984) Characterization of recognition sites on bacteriophage HP1c1 DNA which interact with the DNA uptake system of Haemophilus influenzae Rd. Gene 31:187–196PubMedCrossRefGoogle Scholar
  67. Forterre P (2002) A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet 18:236–723PubMedCrossRefGoogle Scholar
  68. Friedrich A, Hartsch T, Averhoff B (2001) Natural transformation in mesophilic and thermophilic bacteria: identification and characterization of novel, closely related competence genes in Acinetobacter sp. strain BD413 and Thermus thermophilus HB27. Appl Environ Microbiol 67:3140–3148PubMedCrossRefGoogle Scholar
  69. Friedrich A, Prust C, Hartsch T et al (2002) Molecular analyses of the natural transformation machinery and identification of pilus structures in the extremely thermophilic bacterium Thermus thermophilus strain HB27. Appl Environ Microbiol 68:745–755PubMedCrossRefGoogle Scholar
  70. Friedrich A, Rumszauer J, Henne A, Averhoff B (2003) Pilin-like proteins in the extremely thermophilic bacterium Thermus thermophilus HB27: implication in competence for natural transformation and links to type IV pilus biogenesis. Appl Environ Microbiol 69:3695–3700PubMedCrossRefGoogle Scholar
  71. Fröls S, Ajon M, Wagner M et al (2008) UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation. Mol Microbiol 70:938–952PubMedCrossRefGoogle Scholar
  72. Fröls S, White MF, Schleper C (2009) Reactions to UV damage in the model archaeon Sulfolobus solfataricus. Biochem Soc Trans 37:36–41PubMedCrossRefGoogle Scholar
  73. Garcia-Vallvé S, Romeu A, Palau J (2000) Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res 10:1719–1725PubMedCrossRefGoogle Scholar
  74. Gaudin M, Gauliard E, Schouten S et al (2012) Hyperthermophilic archaea produce membrane vesicles that can transfer DNA. Environ Microbiol Rep 5:109–116PubMedCrossRefGoogle Scholar
  75. Geslin C, Le Romancer M, Erauso G et al (2003) PAV1, the first virus-like particle isolated from a hyperthermophilic Euryarchaeote, “Pyrococcus abyssi”. J Bacteriol 185:3888–3894PubMedCrossRefGoogle Scholar
  76. Geslin C, Gaillard M, Flament D et al (2007) Analysis of the first genome of a hyperthermophilic marine virus-like particle, PAV1, isolated from Pyrococcus abyssi. J Bacteriol 189:4510–4519PubMedCrossRefGoogle Scholar
  77. Ghane F, Grogan DW (1998) Chromosomal marker exchange in the thermophilic archaeon Sulfolobus acidocaldarius: physiological and cellular aspects. Microbiology 144:1649–1657CrossRefGoogle Scholar
  78. Gomis-Rüth FX, Coll M (2006) Cut and move: protein machinery for DNA processing in bacterial conjugation. Curr Opin Struct Biol 16:744–772PubMedCrossRefGoogle Scholar
  79. Gorlas A, Koonin EV, Bienvenu N et al (2012) TPV1, the first virus isolated from the hyperthermophilic genus Thermococcus. Environ Microbiol 14:503–516PubMedCrossRefGoogle Scholar
  80. Gounder K, Brzuszkiewicz E, Liesegang H et al (2011) Sequence of the hyperplastic genome of the naturally competent Thermus scotoductus SA-01. BMC Genomics 12:577PubMedCrossRefGoogle Scholar
  81. Greve B, Jensen S, Brügger K et al (2004) Genomic comparison of archaeal conjugative plasmids from Sulfolobus. Archaea 1:231–239PubMedCrossRefGoogle Scholar
  82. Gribaldo S, Brochier-Armanet C (2006) The origin and evolution of Archaea: a state of the art. Philos Trans R Soc Lond B Biol Sci 361:1007–1022PubMedCrossRefGoogle Scholar
  83. Grogan DW (1996) Exchange of genetic markers at extremely high temperatures in the archaeon Sulfolobus acidocaldarius. J Bacteriol 178:3207–3211PubMedGoogle Scholar
  84. Grogan DW, Stengel KR (2008) Recombination of synthetic oligonucleotides with prokaryotic chromosomes: substrate requirements of the Escherichia coli/lambdaRed and Sulfolobus acidocaldarius recombination systems. Mol Microbiol 69:1255–1265PubMedCrossRefGoogle Scholar
  85. Grogan DW, Carver GT, Drake JW (2001) Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc Natl Acad Sci USA 98:7928–7933PubMedCrossRefGoogle Scholar
  86. Guglielmini J, Quintais L, Garcillán-Barcia MP et al (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7:e1002222PubMedCrossRefGoogle Scholar
  87. Guglielmini J, de la Cruz F, Rocha EPC (2013) Evolution of conjugation and Type IV secretion systems. Mol Biol Evol 30:315–331PubMedCrossRefGoogle Scholar
  88. Guiral S, Mitchell TJ, Martin B, Claverys J-P (2005) Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc Natl Acad Sci USA 102:8710–8715PubMedCrossRefGoogle Scholar
  89. Halary S, Leigh JW, Cheaib B et al (2010) Network analyses structure genetic diversity in independent genetic worlds. Proc Natl Acad Sci USA 107:127–132PubMedCrossRefGoogle Scholar
  90. Happonen LJ, Redder P, Peng X et al (2010) Familial relationships in hyperthermo- and acidophilic archaeal viruses. J Virol 84:4747–4754PubMedCrossRefGoogle Scholar
  91. Håvarstein LS, Martin B, Johnsborg O et al (2006) New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. Mol Microbiol 59:1297–1307PubMedCrossRefGoogle Scholar
  92. Heine M, Chandra SBC (2009) The linkage between reverse gyrase and hyperthermophiles: a review of their invariable association. J Microbiol 47:229–234PubMedCrossRefGoogle Scholar
  93. Held NL, Whitaker RJ (2009) Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ Microbiol 11:457–466PubMedCrossRefGoogle Scholar
  94. Herriott RM, Meyer EM, Vogt M (1970) Defined nongrowth media for stage II development of competence in Haemophilus influenzae. J Bacteriol 101:517–524PubMedGoogle Scholar
  95. Hidaka Y, Hasegawa M, Nakahara T, Hoshino T (1994) The entire population of Thermus thermophilus cells is always competent at any growth phase. Biosci Biotechnol Biochem 58:1338–1339PubMedCrossRefGoogle Scholar
  96. Hofreuter D, Odenbreit S, Püls J et al (2000) Genetic competence in Helicobacter pylori: mechanisms and biological implications. Res Microbiol 151:487–491Google Scholar
  97. Jaatinen ST, Happonen LJ, Laurinmäki P et al (2008) Biochemical and structural characterisation of membrane-containing icosahedral dsDNA bacteriophages infecting thermophilic Thermus thermophilus. Virology 379:10–19PubMedCrossRefGoogle Scholar
  98. Jain R, Rivera MC, Moore JE, Lake JA (2003) Horizontal gene transfer accelerates genome innovation and evolution. Mol Biol Evol 20:1598–1602PubMedCrossRefGoogle Scholar
  99. Jalasvuori M, Jaatinen ST, Laurinavicius S et al (2009) The closest relatives of icosahedral viruses of thermophilic bacteria are among viruses and plasmids of the halophilic archaea. J Virol 83:9388–9397PubMedCrossRefGoogle Scholar
  100. Johnsborg O, Eldholm V, Håvarstein LS (2007) Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol 158:767–778PubMedCrossRefGoogle Scholar
  101. Jonuscheit M, Martusewitsch E, Stedman KM, Schleper C (2003) A reporter gene system for the hyperthermophilic archaeon Sulfolobus solfataricus based on a selectable and integrative shuttle vector. Mol Microbiol 48:1241–1252PubMedCrossRefGoogle Scholar
  102. Jorth P, Whiteley M (2012) An evolutionary link between natural transformation and CRISPR adaptive immunity. mBio 3:Google Scholar
  103. Kahn ME, Maul G, Goodgal SH (1982) Possible mechanism for donor DNA binding and transport in Haemophilus. Proc Natl Acad Sci USA 79:6370–6374PubMedCrossRefGoogle Scholar
  104. Kampmann M, Stock D (2004) Reverse gyrase has heat-protective DNA chaperone activity independent of supercoiling. Nucleic Acids Res 32:3537–3545PubMedCrossRefGoogle Scholar
  105. Kikuchi A, Asai K (1984) Reverse gyrase—a topoisomerase which introduces positive superhelical turns into DNA. Nature 309:677–681PubMedCrossRefGoogle Scholar
  106. Koerdt A, Gödeke J, Berger J et al (2010) Crenarchaeal biofilm formation under extreme conditions. PLoS ONE 5:e14104PubMedCrossRefGoogle Scholar
  107. Kolling GL, Matthews KR (1999) Export of virulence genes and shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl Environ Microbiol 65:1843–1848PubMedGoogle Scholar
  108. König H, Messner P, Stetter KO (1988) The fine structure of the fibers of Pyrodictium occultum. FEMS Microbiol Lett 49:207–212CrossRefGoogle Scholar
  109. Koonin EV (2009) On the origin of cells and viruses: primordial virus world scenario. Ann NY Acad Sci 1178:47–64PubMedCrossRefGoogle Scholar
  110. Koonin EV, Wolf YI (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36:6688–6719PubMedCrossRefGoogle Scholar
  111. Koyama Y, Hoshino T, Tomizuka N, Furukawa K (1986) Genetic transformation of the extreme thermophile Thermus thermophilus and of other Thermus spp. J Bacteriol 166:338–340PubMedGoogle Scholar
  112. Krüger N-J, Stingl K (2011) Two steps away from novelty—principles of bacterial DNA uptake. Mol Microbiol 80:860–867PubMedCrossRefGoogle Scholar
  113. Krupovic M, Bamford DH (2008) Archaeal proviruses TKV4 and MVV extend the PRD1-adenovirus lineage to the phylum Euryarchaeota. Virology 375:292–300PubMedCrossRefGoogle Scholar
  114. Krupovic M, Forterre P, Bamford DH (2010) Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J Mol Biol 397:144–160PubMedCrossRefGoogle Scholar
  115. Krupovic M, Prangishvili D, Hendrix RW, Bamford DH (2011) Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol Mol Biol Rev 75:610–635PubMedCrossRefGoogle Scholar
  116. Krupovic M, Gonnet M, Hania WB et al (2013) Insights into dynamics of mobile genetic elements in hyperthermophilic environments from five new Thermococcus plasmids. PLoS ONE 8:e49044PubMedCrossRefGoogle Scholar
  117. Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163–184PubMedCrossRefGoogle Scholar
  118. Lang AS, Zhaxybayeva O, Beatty JT (2012) Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol 10:472–482PubMedGoogle Scholar
  119. Lawley T, Klimke W, Gubbins M, Frost L (2003) F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 224:1–15PubMedCrossRefGoogle Scholar
  120. Lawrence JG, Ochman H (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95:9413–9417PubMedCrossRefGoogle Scholar
  121. Levin BR (1981) Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99:1–23PubMedGoogle Scholar
  122. Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715PubMedCrossRefGoogle Scholar
  123. Lipps G (2006) Plasmids and viruses of the thermoacidophilic crenarchaeote Sulfolobus. Extremophiles 10:17–28PubMedCrossRefGoogle Scholar
  124. Lipscomb GL, Stirrett K, Schut GJ et al (2011) Natural competence in the hyperthermophilic archaeon Pyrococcus furiosus facilitates genetic manipulation: construction of markerless deletions of genes encoding the two cytoplasmic hydrogenases. Appl Environ Microbiol 77:2232–2238CrossRefPubMedGoogle Scholar
  125. Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602PubMedGoogle Scholar
  126. MacFadyen LP, Chen D, Vo HC et al (2001) Competence development by Haemophilus influenzae is regulated by the availability of nucleic acid precursors. Mol Microbiol 40:700–707PubMedCrossRefGoogle Scholar
  127. Maier B, Potter L, So M et al (2002) Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci USA 99:16012–16017PubMedCrossRefGoogle Scholar
  128. Majewski J, Cohan FM (1998) The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics 148:13–18PubMedGoogle Scholar
  129. Majewski J, Cohan FM (1999) Adapt globally, act locally: the effect of selective sweeps on bacterial sequence diversity. Genetics 152:1459–1474PubMedGoogle Scholar
  130. Marguet E, Gaudin M, Gauliard E et al (2013) Membrane vesicles, nanopods and/or nanotubes produced by hyperthermophilic archaea of the genus Thermococcus. Biochem Soc Trans 41:436–442PubMedCrossRefGoogle Scholar
  131. Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845PubMedCrossRefGoogle Scholar
  132. Martin B, García P, Castanié MP, Claverys JP (1995) The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls lysogenic induction. Mol Microbiol 15:367–379PubMedCrossRefGoogle Scholar
  133. Mashburn-Warren LM, Whiteley M (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61:839–846PubMedCrossRefGoogle Scholar
  134. Matsushita I, Yanase H (2009) A novel insertion sequence transposed to thermophilic bacteriophage {phi}IN93. J Biochem 146:797–803PubMedCrossRefGoogle Scholar
  135. McDaniel LD, Young E, Delaney J et al (2010) High frequency of horizontal gene transfer in the oceans. Science 330:50PubMedCrossRefGoogle Scholar
  136. Meibom KL, Blokesch M, Dolganov NA et al (2005) Chitin induces natural competence in Vibrio cholerae. Science 310:1824–1827PubMedCrossRefGoogle Scholar
  137. Mell JC, Hall IM, Redfield RJ (2012) Defining the DNA uptake specificity of naturally competent Haemophilus influenzae. Nucleic Acids Res 40:8536–8549PubMedCrossRefGoogle Scholar
  138. Michod RE, Wojciechowski MF, Hoelzer MA (1988) DNA repair and the evolution of transformation in the bacterium Bacillus subtilis. Genetics 118:31–39PubMedGoogle Scholar
  139. Minakhin L, Goel M, Berdygulova Z et al (2008) Genome comparison and proteomic characterization of Thermus thermophilus bacteriophages P23-45 and P74-26: siphoviruses with triplex-forming sequences and the longest known tails. J Mol Biol 378:468–480PubMedCrossRefGoogle Scholar
  140. Mortier-Barrière I, Velten M, Dupaigne P et al (2007) A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 130:824–836PubMedCrossRefGoogle Scholar
  141. Murray NE (2002) Immigration control of DNA in bacteria: self versus non-self. Microbiology 148:3–20PubMedGoogle Scholar
  142. Muskhelishvili G, Palm P, Zillig W (1993) SSV1-encoded site-specific recombination system in Sulfolobus shibatae. Mol Gen Genet 237:334–342PubMedGoogle Scholar
  143. Nakamura Y, Itoh T, Matsuda H, Gojobori T (2004) Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 36:760–766PubMedCrossRefGoogle Scholar
  144. Napoli A, Valenti A, Salerno V et al (2004) Reverse gyrase recruitment to DNA after UV light irradiation in Sulfolobus solfataricus. J Biol Chem 279:33192–33198PubMedCrossRefGoogle Scholar
  145. Naryshkina T, Liu J, Florens L et al (2006) Thermus thermophilus bacteriophage phiYS40 genome and proteomic characterization of virions. J Mol Biol 364:667–677PubMedCrossRefGoogle Scholar
  146. Nesbø CL, L’Haridon S, Stetter KO, Doolittle WF (2001) Phylogenetic analyses of two “Archaeal” genes in Thermotoga maritima reveal multiple transfers between archaea and bacteria. Mol Biol Evol 18:362–375PubMedCrossRefGoogle Scholar
  147. Nickell S, Hegerl R, Baumeister W, Rachel R (2003) Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography. J Struct Biol 141:34–42PubMedCrossRefGoogle Scholar
  148. Norman A, Hansen LH, Sørensen SJ (2009) Conjugative plasmids: vessels of the communal gene pool. Philos Trans R Soc Lond B Biol Sci 364:2275–2289PubMedCrossRefGoogle Scholar
  149. Nunn DN, Lory S (1991) Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc Natl Acad Sci USA 88:3281–3285PubMedCrossRefGoogle Scholar
  150. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304PubMedCrossRefGoogle Scholar
  151. Omelchenko MV, Wolf YI, Gaidamakova EK et al (2005) Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance. BMC Evol Biol 5:57PubMedCrossRefGoogle Scholar
  152. Onai K, Morishita M, Kaneko T et al (2004) Natural transformation of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1: a simple and efficient method for gene transfer. Mol Gen Genet 271:50–59CrossRefGoogle Scholar
  153. Oshima T, Imahori K (1974) Description of Thermus thermophilus (Yoshida and Oshima) comb. nov., a nonsporulating thermophilic bacterium from a Japanese thermal spa. Int J Syst Bacteriol 24:102–112CrossRefGoogle Scholar
  154. Palchevskiy V, Finkel SE (2006) Escherichia coli competence gene homologs are essential for competitive fitness and the use of DNA as a nutrient. J Bacteriol 188:3902–3910PubMedCrossRefGoogle Scholar
  155. Palchevskiy V, Finkel SE (2009) A role for single-stranded exonucleases in the use of DNA as a nutrient. J Bacteriol 191:3712–3716PubMedCrossRefGoogle Scholar
  156. Pallen MJ, Wren BW (2007) Bacterial pathogenomics. Nature 449:835–842PubMedCrossRefGoogle Scholar
  157. Palm P, Schleper C, Grampp B et al (1991) Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 185:242–250PubMedCrossRefGoogle Scholar
  158. Peng X, Blum H, She Q et al (2001) Sequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses. Virology 291:226–234PubMedCrossRefGoogle Scholar
  159. Pérez-Cruz C, Carrión O, Delgado L et al (2013) A new type of outer membrane vesicles produced by the Gram-negative bacterium Shewanella vesiculosa M7T: implications for DNA content. Appl Environ Microbiol AEM. doi:  10.1128/AEM.03657-12
  160. Pérez-Mendoza D, de la Cruz F (2009) Escherichia coli genes affecting recipient ability in plasmid conjugation: are there any? BMC Genomics 10:71PubMedCrossRefGoogle Scholar
  161. Popa O, Dagan T (2011) Trends and barriers to lateral gene transfer in prokaryotes. Curr Opin Microbiol 14:615–623PubMedCrossRefGoogle Scholar
  162. Prangishvili D, Albers SV, Holz I et al (1998) Conjugation in archaea: frequent occurrence of conjugative plasmids in Sulfolobus. Plasmid 40:190–202PubMedCrossRefGoogle Scholar
  163. Prangishvili D, Holz I, Stieger E et al (2000) Sulfolobicins, specific proteinaceous toxins produced by strains of the extremely thermophilic archaeal genus Sulfolobus. J Bacteriol 182:2985–2988PubMedCrossRefGoogle Scholar
  164. Prangishvili D, Forterre P, Garrett RA (2006a) Viruses of the Archaea: a unifying view. Nat Rev Microbiol 4:837–848PubMedCrossRefGoogle Scholar
  165. Prangishvili D, Garrett RA, Koonin EV (2006b) Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res 117:52–67PubMedCrossRefGoogle Scholar
  166. Provvedi R, Dubnau D (1999) ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Mol Microbiol 31:271–280PubMedCrossRefGoogle Scholar
  167. Puigbò P, Wolf YI, Koonin EV (2010) The tree and net components of prokaryote evolution. Genome Biol Evol 2:745–756PubMedCrossRefGoogle Scholar
  168. Rachel R, Wyschkony I, Riehl S, Huber H (2002) The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1:9–18PubMedCrossRefGoogle Scholar
  169. Ramírez-Arcos S, Fernández-Herrero LA, Marín I, Berenguer J (1998) Anaerobic growth, a property horizontally transferred by an Hfr-like mechanism among extreme thermophiles. J Bacteriol 180:3137–3143PubMedGoogle Scholar
  170. Redder P, Peng X, Brügger K et al (2009) Four newly isolated fuselloviruses from extreme geothermal environments reveal unusual morphologies and a possible interviral recombination mechanism. Environ Microbiol 11:2849–2862PubMedCrossRefGoogle Scholar
  171. Redfield RJ (1988) Evolution of bacterial transformation: is sex with dead cells ever better than no sex at all? Genetics 119:213–221PubMedGoogle Scholar
  172. Redfield RJ (1993a) Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J Hered 84:400–404PubMedGoogle Scholar
  173. Redfield RJ (1993b) Evolution of natural transformation: testing the DNA repair hypothesis in Bacillus subtilis and Haemophilus influenzae. Genetics 133:755–761PubMedGoogle Scholar
  174. Redfield RJ, Schrag MR, Dean AM (1997) The evolution of bacterial transformation: sex with poor relations. Genetics 146:27–38PubMedGoogle Scholar
  175. Renelli M, Matias V, Lo RY, Beveridge TJ (2004) DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150:2161–2169PubMedCrossRefGoogle Scholar
  176. Rosenshine I, Tchelet R, Mevarech M (1989) The mechanism of DNA transfer in the mating system of an archaebacterium. Science 245:1387–1389PubMedCrossRefGoogle Scholar
  177. Rumbo C, Fernández-Moreira E, Merino M et al (2011) Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: a new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii. Antimicrob Ag Chemother 55:3084–3090CrossRefGoogle Scholar
  178. Rumszauer J, Schwarzenlander C, Averhoff B (2006) Identification, subcellular localization and functional interactions of PilMNOWQ and PilA4 involved in transformation competency and pilus biogenesis in the thermophilic bacterium Thermus thermophilus HB27. FEBS J 273:3261–3272PubMedCrossRefGoogle Scholar
  179. Sakaki Y, Oshima T (1975) Isolation and characterization of a bacteriophage infectious to an extreme thermophile, Thermus thermophilus HB8. J Virol 15:1449–1453PubMedGoogle Scholar
  180. Santangelo TJ, Cubonová L, Reeve JN (2008) Shuttle vector expression in Thermococcus kodakaraensis: contributions of cis elements to protein synthesis in a hyperthermophilic archaeon. Appl Environ Microbiol 74:3099–3104PubMedCrossRefGoogle Scholar
  181. Santangelo TJ, Cubonová L, Reeve JN (2010) Thermococcus kodakarensis genetics: TK1827-encoded beta-glycosidase, new positive-selection protocol, and targeted and repetitive deletion technology. Appl Environ Microbiol 76:1044–1052PubMedCrossRefGoogle Scholar
  182. Sato T, Fukui T, Atomi H, Imanaka T (2003) Targeted gene disruption by homologous recombination in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Bacteriol 185:210–220PubMedCrossRefGoogle Scholar
  183. Sato T, Fukui T, Atomi H, Imanaka T (2005) Improved and versatile transformation system allowing multiple genetic manipulations of the hyperthermophilic archaeon Thermococcus kodakaraensis. Appl Environ Microbiol 71:3889–3899PubMedCrossRefGoogle Scholar
  184. Schleper C, Holz I, Janekovic D et al (1995) A multicopy plasmid of the extremely thermophilic archaeon Sulfolobus effects its transfer to recipients by mating. J Bacteriol 177:4417–4426PubMedGoogle Scholar
  185. Schmidt KJ, Beck KE, Grogan DW (1999) UV stimulation of chromosomal marker exchange in Sulfolobus acidocaldarius: implications for DNA repair, conjugation and homologous recombination at extremely high temperatures. Genetics 152:1407–1415PubMedGoogle Scholar
  186. Schröder G, Lanka E (2005) The mating pair formation system of conjugative plasmids-A versatile secretion machinery for transfer of proteins and DNA. Plasmid 54:1–25PubMedCrossRefGoogle Scholar
  187. Schwarzenlander C, Averhoff B (2006) Characterization of DNA transport in the thermophilic bacterium Thermus thermophilus HB27. FEBS J 273:4210–4218PubMedCrossRefGoogle Scholar
  188. Schwarzenlander C, Haase W, Averhoff B (2009) The role of single subunits of the DNA transport machinery of Thermus thermophilus HB27 in DNA binding and transport. Environ Microbiol 11:801–808PubMedCrossRefGoogle Scholar
  189. Sedwick P, Stuben D (1996) Chemistry of shallow submarine warm springs in an arc-volcanic setting: Volcano Island, Aeolian Archipelago, Italy. Mar Chem 53:15CrossRefGoogle Scholar
  190. Seitz P, Blokesch M (2012) Cues and regulatory pathways involved in natural competence and transformation in pathogenic and environmental Gram-negative bacteria. FEMS Microbiol Rev 37:336–363Google Scholar
  191. She Q, Phan H, Garrett RA et al (1998) Genetic profile of pNOB8 from Sulfolobus: the first conjugative plasmid from an archaeon. Extremophiles 2:417–425PubMedCrossRefGoogle Scholar
  192. She Q, Shen B, Chen L (2004) Archaeal integrases and mechanisms of gene capture. Biochem Soc Trans 32:222–226PubMedCrossRefGoogle Scholar
  193. She Q, Zhu H, Xiang X (2006) Integration mechanisms: possible role in genome evolution. In: Garrett RA, Klenk H-P (eds) Archaea. Blackwell Publishing Ltd, Malden, pp 113–124CrossRefGoogle Scholar
  194. Shetty A, Chen S, Tocheva EI et al (2011) Nanopods: a new bacterial structure and mechanism for deployment of outer membrane vesicles. PLoS ONE 6:e20725PubMedCrossRefGoogle Scholar
  195. Siebers B, Zaparty M, Raddatz G et al (2011) The complete genome sequence of Thermoproteus tenax: a physiologically versatile member of the Crenarchaeota. PLoS ONE 6:e24222PubMedCrossRefGoogle Scholar
  196. Silverman PM (1997) Towards a structural biology of bacterial conjugation. Mol Microbiol 23:423–429PubMedCrossRefGoogle Scholar
  197. Soler N, Marguet E, Verbavatz J-M, Forterre P (2008) Virus-like vesicles and extracellular DNA produced by hyperthermophilic archaea of the order Thermococcales. Res Microbiol 159:390–399PubMedCrossRefGoogle Scholar
  198. Soler N, Gaudin M, Marguet E, Forterre P (2011) Plasmids, viruses and virus-like membrane vesicles from Thermococcales. Biochem Soc Trans 39:36–44PubMedCrossRefGoogle Scholar
  199. Stedman KM, She Q, Phan H et al (2000) pING family of conjugative plasmids from the extremely thermophilic archaeon Sulfolobus islandicus: insights into recombination and conjugation in Crenarchaeota. J Bacteriol 182:7014–7020PubMedCrossRefGoogle Scholar
  200. Stetter KO (2006a) Hyperthermophiles in the history of life. Philos Trans R Soc Lond B Biol Sci 361:1837–1843PubMedCrossRefGoogle Scholar
  201. Stetter KO (2006b) History of discovery of the first hyperthermophiles. Extremophiles 10:357–362PubMedCrossRefGoogle Scholar
  202. Stetter KO (2013) A brief history of the discovery of hyperthermophilic life. Biochem Soc Trans 41:416–420PubMedCrossRefGoogle Scholar
  203. Stingl K, Muller S, Scheidgen-Kleyboldt G et al (2009) Composite system mediates two-step DNA uptake into Helicobacter pylori. Proc Natl Acad Sci USA 107:1184–1189 Google Scholar
  204. Suckow G, Seitz P, Blokesch M (2011) Quorum sensing contributes to natural transformation of Vibrio cholerae in a species-specific manner. J Bacteriol 193:4914–4924PubMedCrossRefGoogle Scholar
  205. Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721PubMedCrossRefGoogle Scholar
  206. Valenti A, De Felice M, Perugino G et al (2012) Synergic and opposing activities of thermophilic RecQ-like helicase and topoisomerase 3 proteins in Holliday junction processing and replication fork stabilization. J Biol Chem 287:30282–30295PubMedCrossRefGoogle Scholar
  207. van Passel MWJ (2008) An intragenic distribution bias of DNA uptake sequences in Pasteurellaceae and Neisseriae. Biol Direct 3:12PubMedCrossRefGoogle Scholar
  208. Vogelmann J, Ammelburg M, Finger C et al (2011) Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE. EMBO J 30:2246–2254PubMedCrossRefGoogle Scholar
  209. Waege I, Schmid G, Thumann S et al (2010) Shuttle vector-based transformation system for Pyrococcus furiosus. Appl Environ Microbiol 76:3308–3313PubMedCrossRefGoogle Scholar
  210. Wang Y, Duan Z, Zhu H et al (2007) A novel Sulfolobus non-conjugative extrachromosomal genetic element capable of integration into the host genome and spreading in the presence of a fusellovirus. Virology 363:124–133PubMedCrossRefGoogle Scholar
  211. Weisburg WG, Giovannoni SJ, Woese CR (1989) The Deinococcus-Thermus phylum and the effect of rRNA composition on phylogenetic tree construction. Syst Appl Microbiol 11:128–134PubMedCrossRefGoogle Scholar
  212. White MF (2011) Homologous recombination in the archaea: the means justify the ends. Biochem Soc Trans 39:15–19PubMedCrossRefGoogle Scholar
  213. White JR, Escobar-Paramo P, Mongodin EF et al (2008) Extensive genome rearrangements and multiple horizontal gene transfers in a population of Pyrococcus isolates from Vulcano Island, Italy. Appl Environ Microbiol 74:6447–6451PubMedCrossRefGoogle Scholar
  214. Wolf YI, Rogozin IB, Kondrashov AS, Koonin EV (2001) Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. Genome Res 11:356–372PubMedCrossRefGoogle Scholar
  215. Wolfgang M, Lauer P, Park HS et al (1998) PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29:321–330PubMedCrossRefGoogle Scholar
  216. Worrell VE, Nagle DP, McCarthy D, Eisenbraun A (1988) Genetic transformation system in the archaebacterium Methanobacterium thermoautotrophicum Marburg. J Bacteriol 170:653–656PubMedGoogle Scholar
  217. Wozniak RAF, Waldor MK (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8:552–563PubMedCrossRefGoogle Scholar
  218. Yaron S, Kolling GL, Simon L, Matthews KR (2000) Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl Environ Microbiol 66:4414–4420PubMedCrossRefGoogle Scholar
  219. Yu MX, Slater MR, Ackermann H-W (2006) Isolation and characterization of Thermus bacteriophages. Arch Virol 151:663–679PubMedCrossRefGoogle Scholar
  220. Zaneveld JR, Nemergut DR, Knight R (2008) Are all horizontal gene transfers created equal? Prospects for mechanism-based studies of HGT patterns. Microbiology 154:1–15PubMedCrossRefGoogle Scholar
  221. Zawadzki P, Roberts MS, Cohan FM (1995) The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics 140:917–932PubMedGoogle Scholar
  222. Zhang C, Krause DJ, Whitaker RJ (2013) Sulfolobus islandicus: a model system for evolutionary genomics. Biochem Soc Trans 41:458–462PubMedCrossRefGoogle Scholar
  223. Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. J Bacteriol 64:679–699PubMedGoogle Scholar

Copyright information

© Springer Japan 2013

Authors and Affiliations

  • Marleen van Wolferen
    • 1
  • Małgorzata Ajon
    • 2
  • Arnold J. M. Driessen
    • 2
  • Sonja-Verena Albers
    • 1
  1. 1.Molecular Biology of ArchaeaMax Planck Institute for Terrestrial MicrobiologyMarburgGermany
  2. 2.Department of Molecular Microbiology, Groningen Biomolecular Sciences and Biotechnology InstituteUniversity of Groningen GroningenThe Netherlands

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