Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-05-07T23:08:15.785Z Has data issue: false hasContentIssue false
  • English
  • Français

Detection of potential transgenic plant DNA recipients among soil bacteria

Published online by Cambridge University Press:  26 October 2007

Jean-Michel Monier ,
Dominique Bernillon ,
Elizabeth Kay ,
Aurélie Faugier ,
Oleksandra Rybalka ,
Yves Dessaux ,
Pascal Simonet  and
Timothy M. Vogel
Jean-Michel Monier
Affiliation:
Écologie Microbienne, Université de Lyon, 69003 Lyon, Lyon I, 69622 Villeurbanne, France Institut des Sciences Végétales, CNRS UMR2235, Gif-sur-Yvette, France Environmental Microbial Genomics Group, Laboratoire Ampère, École Centrale de Lyon, 69134 Ecully, France
Dominique Bernillon
Affiliation:
Écologie Microbienne, Université de Lyon, 69003 Lyon, Lyon I, 69622 Villeurbanne, France
Elizabeth Kay
Affiliation:
Écologie Microbienne, Université de Lyon, 69003 Lyon, Lyon I, 69622 Villeurbanne, France
Aurélie Faugier
Affiliation:
Écologie Microbienne, Université de Lyon, 69003 Lyon, Lyon I, 69622 Villeurbanne, France Environmental Microbial Genomics Group, Laboratoire Ampère, École Centrale de Lyon, 69134 Ecully, France
Oleksandra Rybalka
Affiliation:
Écologie Microbienne, Université de Lyon, 69003 Lyon, Lyon I, 69622 Villeurbanne, France Environmental Microbial Genomics Group, Laboratoire Ampère, École Centrale de Lyon, 69134 Ecully, France
Yves Dessaux
Affiliation:
Institut des Sciences Végétales, CNRS UMR2235, Gif-sur-Yvette, France
Pascal Simonet
Affiliation:
Écologie Microbienne, Université de Lyon, 69003 Lyon, Lyon I, 69622 Villeurbanne, France Environmental Microbial Genomics Group, Laboratoire Ampère, École Centrale de Lyon, 69134 Ecully, France
Timothy M. Vogel
Affiliation:
Écologie Microbienne, Université de Lyon, 69003 Lyon, Lyon I, 69622 Villeurbanne, France Environmental Microbial Genomics Group, Laboratoire Ampère, École Centrale de Lyon, 69134 Ecully, France

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The likelihood of gene transfer from transgenic plants to bacteria is dependent on gene number and the presence of homologous sequences. The large number of transgene copies in transplastomic (transgenes contained in the chloroplast genome) plant cells as well as the prokaryotic origin of the transgene, may thus significantly increase the likelihood of gene transfer to bacteria that colonize plant tissues. In order to assess the probability of such transfer, the length of homologous DNA sequences required between the transgene and the genome of the bacterial host was assessed. In addition, the probability that bacteria, which co-infect diseased plants, are transformable and have sequences similar to the flanking regions of the transgene was evaluated. Using Acinetobacter baylyi strain BD143 and transplastomic tobacco plants harboring the aadA gene (streptomycin and spectinomycin resistance), we found that sequences identical to the flanking regions containing as few as 55 nucleotides were sufficient for recombination to occur. Consequently, a collection of bacterial isolates able to colonize tobacco plant tissue infected by Ralstonia solanacearum strain K60 was obtained, screened for DNA sequence similarity with the chloroplastic genes accD and rbcL flanking the transgene, and tested for their ability to uptake extracellular DNA (broad host-range pBBR1MCS plasmids) by natural or electro-transformation. Results showed that among the 288 bacterial isolates tested, 8% presented DNA sequence similarity with one or both chloroplastic regions flanking the transgene. Two isolates, identified as Pseudomonas sp. and Acinetobacter sp., were able to integrate exogenous plasmid DNA by electro-transformation and natural transformation, respectively. Our data suggest that transplastomic plant DNA recipients might be present in soil bacterial communities.

Keywords

GMOtransplastomictransgenenatural transformationrecombinationhybridizationDNAantibiotic resistance genesoiltobaccobacteriaAcinetobacterRalstonia
Type
Research Article
Information
Environmental Biosafety Research , Volume 6 , Issue 1-2: Thematic Issue on Horizontal Gene Transfer , January 2007 , pp. 71 - 83
Copyright
© ISBR, EDP Sciences, 2007

References

Antoine, R, Locht, C (1992) Isolation and molecular characterization of a novel broad-host-range plasmid from Bordetella bronchiseptica with sequence similarities to plasmids from gram-positive organisms. Mol. Microbiol. 6: 1785–1799 CrossRef
Bertolla F, Van Gijsegem F, Nesme X, Simonet P (1997) Conditions for natural transformation of Ralstonia solanacearum. Appl. Environ. Microbiol. 63: 4965–4968
Bertrand, H, Poly, F, Tran Van, V, Lombard, N, Nalin, R, Vogel, TM, Simonet, P (2005) High molecular weight DNA recovery from soils prerequisite for biotechnological metagenomic library construction. J. Microbiol. Methods 62: 1–11 CrossRef
Binnewies, TT, Motro, Y, Hallin, PF, Lund, O, Dunn, D, La, T, Hampson, DJ, Bellgard, M, Wassenaar, TM, Ussery, DW (2006) Ten years of bacterial genome sequencing: comparative-genomics-based discoveries. Funct. Integr. Genomics 6: 165–185 CrossRef
Boucher, CA, Barberis, PA, Trigalet, AP, Demery, DA (1985) Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5 induced avirulent mutants. J. Gen. Microbiol. 131: 2449–2457
Broothaerts, W, Mitchell, HJ, Weir, B, Kaines, S, Smith, LMA, Yang, W, Mayer, JE, Roa-Rodriguez, C, Jefferson, RA (2005) Gene transfer to plants by diverse species of bacteria. Nature 433: 629–633 CrossRef
Buddenhagen, I, Kelman, A (1964) Biological and physiological aspects of bacterial wilt caused by Pseudomonas solanacearum. Ann. Rev. Phytopathol. 2: 203–230 CrossRef
Ceccherini, M, Pote, J, Kay, E, Van, VT, Marechal, J, Pietramellara, G, Nannipieri, P, Vogel, TM, Simonet, P (2003) Degradation and transformability of DNA from transgenic leaves. Appl. Environ. Microbiol. 69: 673–678 CrossRef
Cérémonie H, Buret F, Simonet P, Vogel TM (2004) Isolation of lightning-competent soil bacteria. Appl. Environ. Microbiol. 70: 6342–6346
Cérémonie, H, Buret, F, Simonet, P, Vogel, TM (2006) Natural electro-transformation of lightning competent Pseudomonas strain in artificial soil microcosms. Appl. Environ. Microbiol. 72: 2385–2389 CrossRef
Courtois S, Frostegard A, Gorensson P, Depret G, Jannin P, Simonet P (2001) Quantification of bacterial subgroups in soil: comparison of DNA extracted directly from soil or from cells previously released by density gradient centrifugation. Environ. Microbiol. 3: 431–439
D'Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311: 374–377
Davison J (2004) Monitoring horizontal gene transfer. Nat. Biotechnol. 22: 1349–1350
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
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
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 CrossRef
de Vries, J, Wackernagel, W (2004) Microbial horizontal gene transfer and the DNA release from transgenic. Plant Soil 266: 91–104 CrossRef
Demanèche S, Bertolla F, Buret F, Nalin R, Sailland A, Auriol P, Vogel TM, Simonet P (2001) Laboratory-scale evidence for lightning-mediated gene transfer in soil. Appl. Environ. Microbiol. 67: 3440–3444
Gebhard F, Smalla K (1998) Transformation of Acinetobacter sp. strain BD413 by transgenic sugar beet DNA. Appl. Environ. Microbiol. 64: 1550–1554
Heinemann JA, Traavik T (2004) Problems in monitoring horizontal gene transfer in field trials of transgenic plants. Nat. Biotechnol. 22: 1105–1109
James C, Krattiger AF (1996) Global review of the field testing and commercialization of transgenic plants: 1986–1995. The first decade of crop biotechnology. ISAAA Briefs No. 1, ISAAA, Ithaca, New York
Juni, E, Janick, A (1969) Transformation of Acinetobacter calcoaceticus. J. Bacteriol. 98: 281–288
Kay E, Bertolla F, Vogel TM, Simonet P (2002a) Opportunistic colonization of Ralstonia solanacearum-infected plants by Acinetobacter sp. and its natural competence development. Microb. Ecol. 43: 291–297
Kay, E, Vogel, TM, Bertolla, F, Nalin, R, Simonet, P (2002b) In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl. Environ. Microbiol. 68: 3345–3351 CrossRef
Kay E, Chabrillat G, Vogel TM, Simonet P (2003) Intergeneric transfer of chromosomal and conjugative plasmid genes between Ralstonia solanacearum and Acinetobacter sp. BD413. Mol. Plant-Microbe Interact. 16: 74–82
Kelman, A (1954) The relationship of pathogenicity of Pseudomonas solanacearum to colony appearance in a tetrazolium medium. Phytopathology 44: 693–695
Khasanov FK, Zhvingila DJ, Zailhudlin AA, Prozorov AA, Bashkirov VI (1992) Homologous recombination between plasmid and chromosomal DNA in Bacillus subtilis requires approximately 70 bp of homology. Mol. Gen. Genet. 234: 494–497
Kovach, ME, Elzer, PH, Hill, DS, Robertson, GT, Farris, MA, Roop, RM, Peterson, KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175–176 CrossRef
Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58: 563–602
Meier P, Wackernagel W (2003) Mechanisms of homology-facilitated illegitimate recombination for foreign DNA acquisition in transformable Pseudomonas stutzeri. Mol. Microbiol. 48: 1107–1118
Miki B, McHugh S (2004) Selectable marker genes in transgenic plants: applications, alternatives and biosafety. J. Biotechnol. 107: 193–232
Morales VM, Baeckman A, Bagdasarian M (1991) A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97: 39–47
Nielsen KM, Townsend JP (2004) Monitoring and modeling horizontal gene transfer. Nature Biotechnol. 22: 1110–1114
Nielsen, KM, Bones, AM, Smalla, K, van Elsas, JD (1998) Horizontal gene transfer from transgenic plants to terrestrial bacteria - a rare event? FEMS Microbiol. Rev. 22: 79–103 CrossRef
Nielsen KM, van Elsas JD, Smalla K (2000) Transformation of Acinetobacter sp. strain BD413(pFG4 ${\rm \Delta}$ nptII) with transgenic plant DNA in soil microcosms and effects of kanamycin on selection of transformants. Appl. Environ. Microbiol. 66: 1237–1242
Palmen, R, Vosman, B, Buijsman, P, Breek, CK, Hellingwerf, KJ (1993) Physiological characterization of natural transformation in Acinetobacter calcoaceticus. J. Gen. Microbiol. 139: 295–305 CrossRef
Pontiroli A, Simonet P, Frostegard A, Vogel TM, Monier JM (2007) Fate of transgenic plant DNA in the environment. Environ. Biosafety Res. 6, doi: 10.1051/ebr:2007037
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 CrossRef
Ray JL, Nielsen KM (2005) Experimental methods for assaying natural transformation and inferring horizontal gene transfer. Methods Enzymol. 224: 491–520
Tepfer D, Garcia-Gonzales R, Mansouri H, Seruga M, Message B, Leach F, Perica MC (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
van Elsas, JD, Turner, S, Bailey, MJ (2003) Horizontal gene transfer in the phytosphere. New Phytol. 157: 525–537 CrossRef