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Molecular aspects of gene transfer and foreign DNA acquisition in prokaryotes with regard to safety issues

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Abstract

Horizontal gene transfer (HGT) is part of prokaryotic life style and a major factor in evolution. In principle, any combinations of genetic information can be explored via HGT for effects on prokaryotic fitness. HGT mechanisms including transformation, conjugation, transduction, and variations of these plus the role of mobile genetic elements are summarized with emphasis on their potential to translocate foreign DNA. Complementarily, we discuss how foreign DNA can be integrated in recipient cells through homologous recombination (HR), illegitimate recombination (IR), and combinations of both, site-specific recombination, and the reconstitution of plasmids. Integration of foreign DNA by IR is very low, and combinations of IR with HR provide intermediate levels compared to the high frequency of homologous integration. A survey of studies on potential HGT from various transgenic plants indicates very rare transfer of foreign DNA. At the same time, in prokaryotic habitats, genes introduced into transgenic plants are abundant, and natural HGT frequencies are relatively high providing a greater chance for direct transfer instead of via transgenic plants. It is concluded that potential HGT from transgenic plants to prokaryotes is not expected to influence prokaryotic evolution and to have negative effects on human or animal health and the environment.

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References

  • Alpert CA, Mater DD, Muller MC, Ouriet MF, Duval-Iflah Y, Corthier G (2003) Worst-case scenarios for horizontal gene transfer from Lactococcus lactis carrying heterologous genes to Enterococcus faecalis in the digestive tract of gnotobiotic mice. Environ Biosafety Res 2:173–180

    CAS  Google Scholar 

  • Ammann A, Neve H, Geis A, Heller KJ (2008) Plasmid transfer via transduction from Streptococcus thermophilus to Lactococcus lactis. J Bacteriol 190:3083–3087

    CAS  Google Scholar 

  • Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD (2005) Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci USA 102:12554–12559

    CAS  Google Scholar 

  • Averhoff B (2009) Shuffling genes around in hot environments: the unique DNA transporter of Thermus thermophilus. FEMS Microbiol Rev 33:611–626

    CAS  Google Scholar 

  • Badosa E, Moreno C, Montesinos E (2004) Lack of detection of ampicillin resistance gene transfer from Bt176 transgenic corn to culturable bacteria under field conditions. FEMS Microbiol Ecol 48:169–178

    CAS  Google Scholar 

  • Bahl MI, Hansen LH, Sørensen SJ (2009) Persistence mechanisms of conjugative plasmids. Methods Mol Biol 532:73–102

    CAS  Google Scholar 

  • Barbe V, Vallenet D, Fonknechten N, Kreimeyer A, Oztas S, Labarre L, Cruveiller S, Robert C, Duprat S, Wincker P, Ornston LN, Weissenbach J, Marliere P, Cohen GN, Medigue C (2004) Unique features revealed by the genome sequence of Acinetobacter sp. ADP1, a versatile and naturally transformation competent bacterium. Nucleic Acids Res 32:5766–5779

    CAS  Google Scholar 

  • Barlow M (2009) What antimicrobial resistance has taught us about horizontal gene transfer. Methods Mol Biol 532:397–411

    CAS  Google Scholar 

  • Barlow M, Hall BG (2002) Phylogenetic analysis shows that the OXA beta-lactamase genes have been on plasmids for millions of years. J Mol Evol 55:314–321

    CAS  Google Scholar 

  • Barth C, Wilczynska Z, Pontes L, Fraser DJ, Fisher PR (1996) Efficient circularization in Escherichia coli of linear plasmid multimers from Dictyostelium discoideum genomic DNA. Plasmid 36:86–94

    CAS  Google Scholar 

  • Beaber JW, Hochhut B, Waldor MK (2004) SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427:72–74

    CAS  Google Scholar 

  • Beiko RG, Ragan MA (2008) Detecting lateral genetic transfer: a phylogenetic approach. Methods Mol Biol 452:457–469

    CAS  Google Scholar 

  • Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA 102:14332–14337

    CAS  Google Scholar 

  • Bellgard MI, Wanchanthuek P, La T, Ryan K, Moolhuijzen P, Albertyn Z, Shaban B, Motro Y, Dunn DS, Schibeci D, Hunter A, Barrero R, Phillips ND, Hampson DJ (2009) Genome sequence of the pathogenic intestinal spirochete Brachyspira hyodysenterica reveals adaptations to its lifestyle in the porcine large intestine. PloS One 4:e4641

    Google Scholar 

  • Bennett PM (2008) Plasmid encoded antibiotic resistance acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 153(Suppl 1):S347–S357

    CAS  Google Scholar 

  • Bennett PM, Livesey CT, Nathwani D, Reeves DS, Saunders JR, Wise R (2004) An assessment of the risks associated with the use of antibiotic resistance genes in genetically modified plants: report of the Working Party of the British Society for Antimicrobial Chemotherapy. J Antimicrob Chemother 53:418–431

    CAS  Google Scholar 

  • Berndt C, Meier P, Wackernagel W (2003) DNA restriction is a barrier to natural transformation in Pseudomonas stutzeri JM300. Microbiology 149:895–901

    CAS  Google Scholar 

  • Bertolla F, Pepin R, Passelegue-Robe E, Paget E, Simkin A, Nesme X, Simonet P (2000) Plant genome complexity may be a factor limiting in situ the transfer of transgenic plant genes to the phytopathogen Ralstonia solanacearum. Appl Environ Microbiol 66:4161–4167

    CAS  Google Scholar 

  • Binh CT, Heuer H, Kaupenjohann M, Smalla K (2008) Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiol Ecol 66:25–37

    CAS  Google Scholar 

  • Bouvier M, Demarre G, Mazel D (2005) Integron cassette insertion: a recombination process involving a folded single strand substrate. EMBO J 24:4356–4367

    CAS  Google Scholar 

  • Boxall AB, Fogg LA, Blackwell PA, Kay P, Pemberton EJ, Croxford A (2004) Veterinary medicines in the environment. Rev Environ Contam Toxicol 180:1–91

    CAS  Google Scholar 

  • Broer I, Dröge-Laser W, Gerke M (1996) Examination of the putative horizontal gene transfer from transgenic plants to Agrobacteria. In: Schmidt ER, Hankeln T (eds) Transgenic organisms and biosafety: horizontal gene transfer, stability of DNA and expression of transgenes. Springer-Verlag, Heidelberg, pp 67–70

    Google Scholar 

  • Brüssow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602

    Google Scholar 

  • Burrus V, Waldor MK (2004) Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 155:376–386

    CAS  Google Scholar 

  • Canchaya C, Fournous G, Brüssow H (2004) The impact of prophages on bacterial chromosomes. Mol Microbiol 53:9–18

    CAS  Google Scholar 

  • Carnoy C, Roten CA (2009) The dif/Xer recombination systems in proteobacteria. PloS One 4:e6531

    Google Scholar 

  • Ceccherini MT, Pote J, Kay E, Van VT, Maréchal J, Pietramellara G, Nannipieri P, Vogel TM, Simonet P (2003) Degradation and transformability of DNA from transgenic leaves. Appl Environ Microbiol 69:673–678

    CAS  Google Scholar 

  • Chen I, Dubnau D (2004) DNA uptake during bacterial transformation. Nature Rev Microbiol 2:241–249

    CAS  Google Scholar 

  • Chen S, Zhao S, White DG, Schroeder CM, Lu R, Yang H, McDermott PF, Ayers S, Meng J (2004) Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol 70:1–7

    CAS  Google Scholar 

  • Cherbas L, Cherbas P (1997) “Parahomologous” gene targeting in Drosophila cells: an efficient, homology-dependent pathway of illegitimate recombination near a target site. Genetics 145:349–358

    CAS  Google Scholar 

  • Choi KH, Kim KJ (2009) Applications of transposon-based gene delivery system in bacteria. J Microbiol Biotechnol 19:217–228

    CAS  Google Scholar 

  • Cohan FM (2002) Sexual isolation and speciation in bacteria. Genetica 116:359–370

    CAS  Google Scholar 

  • Courvalin P (2008) Predictable and unpredictable evolution of antibiotic resistance. J Intern Med 264:4–16

    CAS  Google Scholar 

  • Davids W, Zhang Z (2008) The impact of horizontal gene transfer in shaping operons and protein interaction networks—direct evidence of preferential attachment. BMC Evol Biol 8:23–35

    Google Scholar 

  • de Vries J, Wackernagel W (1998) Detection of nptII (kanamycin resistance) genes in genomes of transgenic plants by marker-rescue transformation. Mol Gen Genet 257:606–613

    Google Scholar 

  • de Vries J, Wackernagel W (2002) Integration of foreign DNA during natural transformation of Acinetobacter sp. by homology-facilitated illegitimate recombination. Proc Natl Acad Sci USA 99:2094–2099

    Google Scholar 

  • de Vries J, Wackernagel W (2004) Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant Soil 266:91–104

    Google Scholar 

  • de Vries J, Meier P, Wackernagel W (2001) The natural transformation of the soil bacteria Pseudomonas stutzeri and Acinetobacter sp. by transgenic plant DNA strictly depends on homologous sequences in the recipient cells. FEMS Microbiol Lett 195:211–215

    Google Scholar 

  • de Vries J, Heine M, Harms K, Wackernagel W (2003) Spread of recombinant DNA by roots and pollen of transgenic potato plants, identified by highly specific biomonitoring using natural transformation of an Acinetobacter sp. Appl Environ Microbiol 69:4455–4462

    Google Scholar 

  • de Vries J, Herzfeld T, Wackernagel W (2004) Transfer of plastid DNA from tobacco to the soil bacterium Acinetobacter sp. by natural transformation. Mol Microbiol 53:323–334

    Google Scholar 

  • Demanèche S, Sanguin H, Poté J, Navarro E, Bernillon D, Mavingui P, Wildi W, Vogel TM, Simonet P (2008) Antibiotic-resistant soil bacteria in transgenic plant fields. Proc Natl Acad Sci USA 105:3957–3962

    Google Scholar 

  • Dill GM (2005) Glyphosate-resistant crops: history, status and future. Pest Manag Sci 61:219–224

    CAS  Google Scholar 

  • Draper O, César CE, Machón C, de la Cruz F, Llosa M (2005) Site-specific recombinase and integrase activities of a conjugative relaxase in recipient cells. Proc Natl Acad Sci USA 102:16385–16390

    CAS  Google Scholar 

  • Dröge M, Pühler A, Selbitschka W (1998) Horizontal gene transfer as a biosafety issue: a natural phenomenon of public concern. J Biotechnol 64:75–90

    Google Scholar 

  • Dufraigne C, Fertil B, Lespinats S, Giron A, Deschavanne P (2005) Detection and characterization of horizontal transfers in prokaryotes using genomic signature. Nucleic Acids Res 33(1):e6

    Google Scholar 

  • Ehrlich SD (1989) Illegitimate recombination in bacteria. In: Berg DE, Howe MM (eds) Mobile DNA. ASM Press, Washington, pp 799–832

    Google Scholar 

  • Frederiksen K, Rosenquist H, Jørgensen K, Wilcks A (2006) Occurrence of natural Bacillus thuringiensis contaminants and residues of Bacillus thuringiensis-based insecticides on fresh fruits and vegetables. Appl Environ Microbiol 72:3435–3440

    CAS  Google Scholar 

  • Gebhard F, Smalla K (1998) Transformation of Acinetobacter sp. strain BD413 by transgenic sugar beet DNA. Appl Environ Microbiol 64:1550–1554

    CAS  Google Scholar 

  • Gebhard F, Smalla K (1999) Monitoring field releases of genetically modified sugar beets for persistence of transgenic plant DNA and horizontal gene transfer. FEMS Microbiol Ecol 28:261–272

    CAS  Google Scholar 

  • Ghosh S, LaPara TM (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic-resistance among soil bacteria. ISME J 1:191–203

    CAS  Google Scholar 

  • Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nature Rev Microbiol 3:679–687

    CAS  Google Scholar 

  • Graupner S, Wackernagel W (1996) Identification of multiple plasmids released from recombinant genomes of Hansenula polymorpha by transformation of Escherichia coli. Appl Environ Microbiol 62:1839–1841

    CAS  Google Scholar 

  • Grindley ND, Whiteson KL, Rice PA (2006) Mechanisms of site-specific recombination. Annu Rev Biochem 75:567–605

    CAS  Google Scholar 

  • Grohmann E, Muth G, Espinosa M (2003) Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67:277–301

    CAS  Google Scholar 

  • Guerra B, Junker E, Schroeter A, Malorny B, Lehmann S, Helmuth R (2003) Phenotypic and genotypic characterization of antimicrobial resistance in German Escherichia coli isolates from cattle, swine and poultry. J Antimicrob Chemother 52:489–492

    CAS  Google Scholar 

  • Guerra B, Junker E, Schroeter A, Helmuth R, Guth BE, Beutin L (2006) Phenotypic and genotypic characterization of antimicrobial resistance in Escherichia coli O111 isolates. J Antimicrob Chemother 57:1210–1214

    CAS  Google Scholar 

  • Harms K, Wackernagel W (2008) The RecBCD and SbcCD DNases suppress homology-facilitated illegitimate recombination during natural transformation of Acinetobacter baylyi. Microbiology 154:2437–2445

    CAS  Google Scholar 

  • Harms K, Schön V, Kickstein E, Wackernagel W (2007) The RecJ DNase strongly suppresses genomic integration of short but not long foreign DNA fragments by homology-facilitated illegitimate recombination during transformation of Acineotbacter baylyi. Mol Microbiol 64:691–702

    CAS  Google Scholar 

  • Havlickova H, Hradecka H, Bernardyova I, Rychlik I (2009) Distribution of integrons and SGI1 among antibiotic resistant Salmonella enterica isolates of animal origin. Vet Microbiol 133:193–198

    CAS  Google Scholar 

  • Heritage J (2005) The fate of transgenes in the human gut. Nature Biotechnol 23:17–21

    CAS  Google Scholar 

  • Heuer H, Krogerrecklenfort E, Wellington EMH, Egan S, van Elsas JD, van Overbeek L, Collard JM, Guillaume G, Karagouni AD, Nikolakopoulou TL, Smalla K (2002) Gentamicin resistance genes in environmental bacteria: prevalence and transfer. FEMS Microbiol Ecol 42:289–302

    CAS  Google Scholar 

  • Hohlweg U, Doerfler W (2001) On the fate of plant or other foreign genes upon the uptake in food or after intramuscular injection in mice. Mol Genet Genomics 265:225–233

    CAS  Google Scholar 

  • Holmfeldt K, Middelboe M, Nybroe O, Riemann L (2007) Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl Environ Microbiol 73:6730–6739

    CAS  Google Scholar 

  • Hughes VM, Datta N (1983) Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era. Nature 302:725–726

    CAS  Google Scholar 

  • Hülter N, Wackernagel W (2008a) Frequent integration of short homologous DNA tracks during Acinetobacter baylyi transformation and influence of transcription and RecJ and SbcCD DNases. Microbiology 154:3676–3685

    Google Scholar 

  • Hülter N, Wackernagel W (2008b) Double illegitimate recombination events integrate DNA segments through two different mechanisms during natural transformation of Acinetobacter baylyi. Mol Microbiol 67:984–995

    Google Scholar 

  • Huys G, Cnockaert M, Vaneechoutte M, Woddford N, Nemec A, Dijkshoorn L, Swings J (2005) Distribution of tetracycline resistance genes in genotypically related and unrelated multiresistant Acinetobacter baumannii strains from different European hospitals. Res Microbiol 156:348–355

    CAS  Google Scholar 

  • Itaya M (1999) Genetic transfer of large DNA inserts to designated loci of the Bacillus subtilis 168 genome. J Bacteriol 181:1045–1048

    CAS  Google Scholar 

  • Iwaki M, Arakawa Y (2006) Transformation of Acinetobacter sp. BD413 with DNA from commercially available genetically modifies potato and papaya. Lett Appl Microbiol 43:215–221

    CAS  Google Scholar 

  • Iwasaki W, Takagi T (2009) Rapid pathway evolution facilitated by horizontal gene transfers across prokaryotic lineages. PloS Genetics 5:1–8

    Google Scholar 

  • Jensen EC, Schrader HS, Rieland B, Thompson TL, Lee KW, Nickerson KW, Kokjohn TA (1998) Prevalence of broad-host-range lytic bacteriophages of Sphaerotilus natans, Escherichia coli, and Pseudomonas aeruginosa. Appl Environ Microbiol 64:575–580

    CAS  Google Scholar 

  • Johnsborg O, Eldholm V, Bjørnstadt ML, Havarstein LS (2008) A predatory mechanism dramatically increases the efficiency of lateral gene transfer in Streptococcus pneumoniae and related commensal species. Mol Microbiol 69:245–253

    CAS  Google Scholar 

  • Joss MJ, Koenig JE, Labbate M, Polz MF, Gillings MR, Stokes HW, Doolittle WF, Boucher Y (2009) ACID: annotation of cassette and integron data. BMC Bioinformatics 10:118–126

    Google Scholar 

  • Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33:376–393

    CAS  Google Scholar 

  • Kaelin P, Gadani F (2000) Occurrence of Bacillus thuringiensis on cured tobacco leaves. Curr Microbiol 40:205–209

    CAS  Google Scholar 

  • Kay E, Vogel TM, Bertolla F, Nalin R, Simonet P (2002) In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl Environ Microbiol 68:3345–3351

    CAS  Google Scholar 

  • Keese P (2008) Risks from GMOs due to horizontal gene transfer. Environ Biosafety Res 7:123–149

    CAS  Google Scholar 

  • Kelly BG, Vespermann A, Bolton DJ (2009) Gene transfer events and their occurrence in selected environments. Food Chem Toxicol 47:978–983

    CAS  Google Scholar 

  • Kharazmi M, Hammes WP, Hertel C (2002) Construction of a marker rescue system in Bacillus subtilis for detection of horizontal gene transfer in food. System Appl Microbiol 25:471–477

    CAS  Google Scholar 

  • Kim MC, Ahn JH, Shin HC, Kim T, Ryu TH, Kim DH, Song HG, Lee GH, Ka JO (2008) Molecular analysis of bacterial community structures in paddy soils for environmental risk assessment with two varieties of genetically modified rice, Iksan 483 and Milyang 204. J Microbiol Biotechnol 18:207–218

    CAS  Google Scholar 

  • Kleter GA, Peijnenburg AA, Aarts HJ (2005) Health considerations regarding horizontal transfer of microbial transgenes present in genetically modified crops. J Biomed Biotechnol 4:326–352

    Google Scholar 

  • Klotz A, Mayer J, Einspanier R (2002) Degradation and possible carry over of feed DNA monitored in pigs and poultry. Eur Food Res Technol 214:271–275

    CAS  Google Scholar 

  • Koonin EV (2007) The biological big bang model for the major transitions in evolution. Biol Direct 2:21

    Google Scholar 

  • Koonin EV, Wolf YI (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36:6688–6719

    CAS  Google Scholar 

  • Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58:401–465

    CAS  Google Scholar 

  • Krzywinska E, Krzywinska J, Schorey JS (2004) Naturally occurring horizontal gene transfer and homologous recombination in Mycobacterium. Microbiology 150:1707–1712

    CAS  Google Scholar 

  • Kunes S, Botstein D, Fox MS (1990) Synapsis-mediated fusion of free DNA ends forms inverted dimer plasmids in yeast. Genetics 124:67–80

    CAS  Google Scholar 

  • Kusano K, Sakagami K, Yokochi T, Naito T, Tokinaga Y, Ueda E, Kobayashi I (1997) A new type of illegitimate recombination is dependent on restriction and homologous interaction. J Bacteriol 179:5380–5390

    CAS  Google Scholar 

  • Labbate M, Case RJ, Stokes HW (2009) The integron/gene cassette system: an active player in bacterial adaptation. Methods Mol Biol 532:103–125

    CAS  Google Scholar 

  • Lang AS, Beatty JT (2007) Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends Microbiol 15:54–62

    CAS  Google Scholar 

  • Larios-Sanz M, Travisano M (2009) Experimental evolution of an essential Bacillus gene in an E. coli host. Methods Mol Biol 532:269–287

    CAS  Google Scholar 

  • Lau SK, Wong GK, Li MW, Woo PC, Yuen KY (2008) Distribution and molecular characterization of tetracycline resistance in Laribacter honkongensis. J Antimicrob Chemother 61:488–497

    CAS  Google Scholar 

  • Lawrence JG, Ochman H (1997) Amelioration of bacteria genomes: rates of change and exchange. J Mol Evol 44:383–397

    CAS  Google Scholar 

  • Lawrence JG, Retchless AC (2009) The interplay of homologous recombination and horizontal gene transfer in bacterial speciation. Methods Mol Biol 532:29–53

    CAS  Google Scholar 

  • Lee CA, Grossman AD (2007) Identification of the origin of transfer (oriT) and DNA relaxase required for conjugation of the integrative and conjugative element ICEBs1 of Bacillus subtilis. J Bacteriol 189:7254–7261

    CAS  Google Scholar 

  • Leplae R, Hebrant A, Wodak SJ, Toussaint A (2004) ACLAME: a classification of mobile genetic elements. Nucleic Acids Res 32:D45–D49

    CAS  Google Scholar 

  • Lercher MJ, Pal C (2008) Integration of horizontal transferred genes into regulatory interaction networks takes many million years. Mol Biol Evol 25:559–567

    CAS  Google Scholar 

  • Lewin A, Jacob D, Freytag B, Appel B (1998) Gene expression in bacteria directed by plant-specific regulatory sequences. Trans Res 7:403–411

    CAS  Google Scholar 

  • Lo CC, Chen SC, Yang JZ (2007) Use of real-time polymerase chain reaction (PCR) and transformation assay to monitor the persistence and bioavailability of transgenic genes released from genetically modified papaya expressing nptII and PRSV genes in the soil. J Agric Food Chem 55:7534–7540

    CAS  Google Scholar 

  • Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602

    CAS  Google Scholar 

  • Lucchini S, Rowley G, Goldberg MD, Hurd D, Harrison M, Hinton JC (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PloS Pathog 2:e81

    Google Scholar 

  • Ma M, Wang H, Yu Y, Zhang D, Liu S (2007) Detection of antimicrobial resistance genes of pathogenic Salmonella from swine with DNA microarray. J Vet Diagn Invest 19:161–167

    Google Scholar 

  • Majewski J (2001) Sexual isolation in bacteria. FEMS Microbiol Lett 199:161–169

    CAS  Google Scholar 

  • Majewski J, Zawadski P, Pickerill P, Cohan FM, Dowson CG (2000) Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation. J Bacteriol 182:1016–1023

    CAS  Google Scholar 

  • Mann BA, Slauch JM (1997) Transduction of low-copy number plasmids by bacteriophage P22. Genetics 146:447–456

    CAS  Google Scholar 

  • Martin PA, Travers RS (1989) Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl Environ Microbiol 55:2437–2442

    Google Scholar 

  • Matic I, Taddei F, Radman M (1996) Genetic barriers among bacteria. Trends Microbiol 4:69–72

    CAS  Google Scholar 

  • Maughan H, Redfield RJ (2009) Extensive variation in natural competence in Haemophilus influenzae. Evolution 63:1852–1866

    Google Scholar 

  • Mazel D (2006) Integrons: agents of bacterial evolution. Nat Rev Microbiol 4:608–620

    CAS  Google Scholar 

  • Meier P, Wackernagel W (2003) Mechanisms of homology-facilitated illegitimate recombination for foreign DNA acquisition in transformable Pseudomonas stutzeri. Mol Microbiol 48:1107–1118

    CAS  Google Scholar 

  • Meier P, Wackernagel W (2005) Impact of mutS inactivation on foreign DNA acquisition by natural transformation in Pseudomonas stutzeri. J Bacteriol 187:143–154

    CAS  Google Scholar 

  • Mercer DK, Scott KP, Melville CM, Glover LA, Flint HJ (2001) Transformation of an oral bacterium via chromosomal integration of free DNA in the presence of human saliva. FEMS Microbiol Lett 200:163–167

    CAS  Google Scholar 

  • Mindlin SZ, Soina VS, Ptrova MA, Gorlenko Z (2008) Isolation of antibiotic resistance bacterial strains from East Siberia permafrost sediments. Genetika 44:36–44

    CAS  Google Scholar 

  • Modrich P, Lahue R (1996) Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem 65:101–133

    CAS  Google Scholar 

  • Monier JM, Bernillon D, Kay E, Faugier A, Rybalka O, Dessaux Y, Simonet P, Vogel TM (2007) Detection of potential transgenic plant DNA recipients among soil bacteria. Environ Biosafety Res 6:71–83

    CAS  Google Scholar 

  • Morris P, Marinelli LJ, Jacobs-Sera D, Hendrix RW, Hatfull GF (2008) Genomic characterization of mycobacteriophage Giles: evidence for phage acquisition of host DNA by illegitimate recombination. J Bacteriol 190:2172–2182

    CAS  Google Scholar 

  • Nagy Z, Chandler M (2004) Regulation of transposition in bacteria. Res Microbiol 155:387–398

    CAS  Google Scholar 

  • Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H, Libby SJ, Fang FC (2006) Selective silencing of foreign DNA with low GC content by H-NS protein in Salmonella. Science 313:236–238

    CAS  Google Scholar 

  • Navarre WW, McClelland M, Libby SJ, Fang FC (2007) Silencing of xenogeneic DNA by H-NS—facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev 21:1456–1471

    CAS  Google Scholar 

  • Nesbø CL, Boucher Y, Dlutek M, Doolittle WF (2005) Lateral gene transfer and phylogenetic assignment of environmental fosmid clones. Environ Microbiol 7:2011–2026

    Google Scholar 

  • Nielsen KM, Gebhard F, Smalla K, Bones AM, van Elsas JD (1997) Evaluation of possible horizontal gene transfer from transgenic plants to the soil bacterium Acinetobacter calcoaceticus BD413. Theor Appl Genet 95:815–821

    CAS  Google Scholar 

  • Nielsen KM, van Elsas JD, Smalla K (2000) Transformation of Acinetobacter sp. strain BD413 (pFG4ΔnptII) with transgenic plant DNA in soil microcosms and effects of kanamycin on selection of transformants. Appl Environ Microbiol 66:1237–1242

    CAS  Google Scholar 

  • Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D (2007) Release and persistence of extracellular DNA in the environment. Environ Biosafety Res 6:37–53

    CAS  Google Scholar 

  • Osborn AM, Böltner D (2002) When phage, plasmids, and transposons collide: genomic islands, and conjugative- and mobilizable-transposons as a mosaic continuum. Plasmid 48:202–212

    Google Scholar 

  • Oshima T, Ishikawa S, Kurokawa K, Aiba H, Ogasawara N (2006) Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13:141–153

    CAS  Google Scholar 

  • Ouoba LI, Lei V, Jensen LB (2008) Resistance of potential probiotic lactic acid bacteria and bifidobacteria of African and European origin to antimicrobials: determination and transferability of the resistance genes to other bacteria. Inter J Food Microbiol 121:217–224

    CAS  Google Scholar 

  • Paget E, Simonet P (1994) On the track of natural transformation in soil. FEMS Microbiol Ecol 15:109–118

    CAS  Google Scholar 

  • Paget E, Lebrun M, Freyssinet G, Simonet P (1998) The fate of recombinant plant DNA in soil. Eur J Soil Biol 34:81–88

    CAS  Google Scholar 

  • Parks AR, Peters JE (2009) Tn7 elements: engendering diversity from chromosomes to episomes. Plasmid 61:1–14

    CAS  Google Scholar 

  • Partridge SR, Tsafnat G, Coiera E, Iredell JR (2009) Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 33:757–784

    CAS  Google Scholar 

  • Peirano G, Agerso Y, Aarestrup FM, dos Prazeres RD (2005) Occurrence of integrons and resistance genes among sulphonamide-resistant Shigella spp. from Brazil. J Antimicrob Chemother 55:301–305

    CAS  Google Scholar 

  • Pontiroli A, Rizzi A, Simonet P, Daffonchio D, Vogel TM, Monier JM (2009) Visual evidence of horizontal gene transfer between plants and bacteria in the phytosphere of transplastomic tobacco. Appl Environ Microbiol 75:3314–3322

    CAS  Google Scholar 

  • Prudhomme M, Libante V, Claverys JP (2002) Homologous recombination at the border: insertion-deletions and the trapping of foreign DNA in Streptococcus pneumoniae. Proc Natl Acad Sci USA 99:2100–2105

    CAS  Google Scholar 

  • Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys JP (2006) Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313:89–92

    CAS  Google Scholar 

  • Radman-Livaja M, Biswas T, Ellenberger T, Landy A, Aihara H (2006) DNA arms do the legwork to ensure the directionality of lambda site-specific recombination. Curr Opin Struct Biol 16:42–50

    CAS  Google Scholar 

  • Rajeev L, Malanowska K, Gardner JF (2009) Challenging a paradigm: the role of DNA homology in tyrosine recombinase reactions. Microbiol Mol Biol Rev 73:300–309

    CAS  Google Scholar 

  • Reznikoff WS (2008) Transposon Tn5. Annu Rev Genet 42:269–286

    CAS  Google Scholar 

  • Ripp S, Miller RV (1995) Effects of suspended particulates on the frequency of transduction among Pseudomonas aeruginosa in a freshwater environment. Appl Environ Microbiol 61:1214–1219

    CAS  Google Scholar 

  • Rizzi A, Brusetti L, Arioli S, Nielsen KM, Tamagnini I, Tamburini A, Sorlini C, Daffonchio D (2008a) Detection of feed-derived maize DNA in goat milk and evaluation of the potential of horizontal transfer to bacteria. Eur Food Res Technol 227:1699–1709

    CAS  Google Scholar 

  • Rizzi A, Pontiroli A, Brusetti L, Borin S, Sorlini C, Abruzzese A, Sacchi GA, Vogel TM, Simonet P, Bazzicalupo M, Nielsen KM, Monier JM, Daffonchio D (2008b) Strategy for in situ detection of natural transformation-based horizontal gene transfer events. Appl Environ Microbiol 74:1250–1254

    CAS  Google Scholar 

  • Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71

    CAS  Google Scholar 

  • Schlüter K, Fütterer J, Potrykus I (1995) “Horizontal” gene transfer from a transgenic potato line to a bacterial pathogen (Erwinia chrysanthemi) occurs—if at all—at an extremely low frequency. Biotechnology 13:1094–1098

    Google Scholar 

  • Schubbert R, Lettmann C, Doerfler W (1994) Ingested foreign (phage M13) DNA survives transiently in the gastrointestinal tract and enters the bloodstream of mice. Mol Gen Genet 242:495–504

    CAS  Google Scholar 

  • Sharan SK, Thomason LC, Kuznetsov SG, Court DL (2009) Recombineering: a homologous recombination-based method of genetic engineering. Nat Protoc 4:206–223

    CAS  Google Scholar 

  • Sharma R, Damgaard D, Alexander TW, Dugan ME, Aalhus JL, Stanford K, McAllister TA (2006) Detection of transgenic and endogenous plant DNA in digesta and tissues of sheep and pigs fed Roundup Ready canola meal. J Agric Food Chem 54:1699–1709

    CAS  Google Scholar 

  • Sikorski J, Graupner S, Lorenz MG, Wackernagel W (1998) Natural genetic transformation of Pseudomonas stutzeri in a nonsterile soil. Microbiology 144:569–576

    CAS  Google Scholar 

  • Sikorski J, Teschner N, Wackernagel W (2002) Highly different levels of natural transformation are associated with genomic subgroups within a local population of Pseudomonas stutzeri from soil. Appl Environ Microbiol 68:865–873

    CAS  Google Scholar 

  • Simpson DJ, Dawson LF, Fry JC, Rogers HJ, Day MJ (2007a) Influence of flanking homology and insert size on the transformation frequency of Acinetobacter baylyi BD413. Environ Biosafety Res 6:55–69

    CAS  Google Scholar 

  • Simpson DJ, Fry JC, Rogers HJ, Day MJ (2007b) Transformation of Acinetobacter baylyi in non-sterile soil using recombinant plant nuclear DNA. Environ Biosafety Res 6:101–112

    CAS  Google Scholar 

  • Smalla K, van Overbeek LS, Pukall R, van Elsas JD (1994) Prevalence of nptII and Tn5 in kanamycin-resistant bacteria from different environments. FEMS Microbiol Ecol 13:47–58

    Google Scholar 

  • Sobecky PA, Coombs JM (2009) Horizontal gene transfer in metal and radionuclide contaminated soils. Methods Mol Biol 532:455–472

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Stanton TB (2007) Prophage-like gene transfer agents—novel mechanisms of gene exchange for Methanococcus, Desulfovibrio, Brachyspira, and Rhodobacter species. Anaerobe 13:43–49

    CAS  Google Scholar 

  • Stedman KM, She Q, Phan H, Holz I, Singh H, Prangishvili D, Garrett R, Zillig W (2000) pING family of conjugative plasmids from the extremely thermophilic archaeon Sulfolobus islandicus: insights into recombination and conjugation in Crenarchaeota. J Bacteriol 182:7014–7020

    CAS  Google Scholar 

  • Stoebel DM, Free A, Dorman CJ (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154:2533–2545

    CAS  Google Scholar 

  • Tepfer D, Garcia-Gonzales R, Mansouri H, Seruga M, Message B, Leach F, Curkovic Perica M (2003) Homology-dependent DNA transfer from plants to a soil bacterium under laboratory conditions: implications in evolution and horizontal gene transfer. Transgenic Res 12:425–437

    CAS  Google Scholar 

  • Thomas CM, Nielsen KM (2005) Mechanism of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721

    CAS  Google Scholar 

  • Tsuru T, Kobayashi I (2008) Multiple genome comparison within a bacterial species reveals a unit of evolution spanning two adjacent genes in a tandem paralog cluster. Mol Biol Evol 25:2457–2473

    CAS  Google Scholar 

  • Tuteja D, Dua M, Khanna R, Dhingra N, Khanna M, Kaur H, Saxena DM, Lal R (2000) The importance of homologous recombination in the generation of large deletions in hybrid plasmids in Amycolatopsis mediterranei. Plasmid 43:1–11

    CAS  Google Scholar 

  • Ubeda C, Maiques E, Knecht E, Lasa I, Novick RP, Penadés JR (2005) Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol 56:836–844

    CAS  Google Scholar 

  • Val ME, Bouvier M, Campos J, Sherratt D, Cornet F, Mazel D, Barre FX (2005) The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae. Mol Cell 19:559–566

    CAS  Google Scholar 

  • Valadares de Amorim G, Whittome B, Shore B, Levin DB (2001) Identification of Bacillus thuringiensis subsp. kurstaki strain HD1-like bacteria from environmental and human samples after aerial spraying of Victoria, British Columbia, Canada, with Foray 48B. Appl Environ Microbiol 67:1035–1043

    CAS  Google Scholar 

  • van den Eede G, Aarts H, Buhk HJ, Corthier G, Flint HJ, Hammes W, Jacobsen B, Midvedt T, van der Vossen J, von Wright A, Wackernagel W, Wilcks A (2004) The relevance of gene transfer to the safety of food and feed derived from genetically modified (GM) plants. Food Chem Toxicol 42:1127–1156

    Google Scholar 

  • Wackernagel W (2006) The various sources and the fate of nucleic acids in soil. In: Nannipieri P, Smalla K (eds) Soil biology, Vol. 8, nucleic acids and proteins in soil. Springer Verlag, Berlin, pp 117–139

    Google Scholar 

  • Wagner T, Arango Isaza LM, Grundmann S, Dörfler U, Schroll R, Schloter M, Hartmann A, Sandermann H, Ernst D (2008) The probability of a horizontal gene transfer from Roundup Ready soybean to root symbiotic bacteria: a risk assessment study on the GSF lysimeter station. Water, Air, & Soil Pollution Focus 8(2):155–162

    CAS  Google Scholar 

  • Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6:1–11

    Google Scholar 

  • Weisberg RA (1996) Specialized transduction. In: Neidhardt FC (ed) Escherichia coli and Salmonella: cellular and molecular biology, Vol 2. ASM Press, Washington, pp 2442–2448

    Google Scholar 

  • Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578–6583

    CAS  Google Scholar 

  • Zaneveld JR, Nemergut DR, Knight R (2008) Are all horizontal gene transfers created equal? Prospects for mechanism-based studies of HGT patterns. Microbiology 154:1–15

    CAS  Google Scholar 

  • Zawadski P, Roberts MS, Cohan FM (1995) The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics 140:917–932

    Google Scholar 

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Acknowledgements

We thank Nils Hülter for help during preparation of the manuscript and Johannes Sikorski for critical reading of the text.

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Brigulla, M., Wackernagel, W. Molecular aspects of gene transfer and foreign DNA acquisition in prokaryotes with regard to safety issues. Appl Microbiol Biotechnol 86, 1027–1041 (2010). https://doi.org/10.1007/s00253-010-2489-3

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