Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T08:38:37.205Z Has data issue: false hasContentIssue false

Release and persistence of extracellular DNAin the environment

Published online by Cambridge University Press:  12 September 2007

Kaare M. Nielsen
Affiliation:
Department of Pharmacy, Faculty of Medicine, University of Tromsø, 9037 Tromsø, Norway Norwegian Institute of Gene Ecology, 9294 Tromsø, Norway
Pål J. Johnsen
Affiliation:
Department of Pharmacy, Faculty of Medicine, University of Tromsø, 9037 Tromsø, Norway
Douda Bensasson
Affiliation:
Faculty of Life Sciences, University of Manchester, Manchester, M13 9PT, UK
Daniele Daffonchio
Affiliation:
Department of Food Science, Technology and Microbiology, University of Milan, Via Celoria 2, 20133 Milan, Italy

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 introduction of genetically modified organisms (GMOs) has called for an improved understanding of the fate of DNA in various environments, because extracellular DNA may also be important for transferring genetic information between individuals and species. Accumulating nucleotide sequence data suggest that acquisition of foreign DNA by horizontal gene transfer (HGT) is of considerable importance in bacterial evolution. The uptake of extracellular DNA by natural transformation is one of several ways bacteria can acquire new genetic information given sufficient size, concentration and integrity of the DNA. We review studies on the release, breakdown and persistence of bacterial and plant DNA in soil, sediment and water, with a focus on the accessibility of the extracellular nucleic acids as substrate for competent bacteria. DNA fragments often persist over time in many environments, thereby facilitating their detection and characterization. Nevertheless, the long-term physical persistence of DNA fragments of limited size observed by PCR and Southern hybridization often contrasts with the short-term availability of extracellular DNA to competent bacteria studied in microcosms. The main factors leading to breakdown of extracellular DNA are presented. There is a need for improved methods for accurately determining the degradation routes and the persistence, integrity and potential for horizontal transfer of DNA released from various organisms throughout their lifecycles.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2007

References

Ahrenholtz, I, Lorenz, MG, Wackernagel, W (1994a) A conditional suicide system in Escherichia coli based on the intracellular degradation of DNA. Appl. Environ. Microbiol. 60: 37463751
Ahrenholtz, I, Lorenz, MG, Wackernagel, W (1994b) The extracellular nuclease of Serratia marcescens: studies on the activity in vitro and effect on transforming DNA in a groundwater aquifer microcosm. Arch. Microbiol. 161: 176183
Alvarez, AJ, Yumet, GM, Santiago, CL, Toranzos, GA (1996) Stability of manipulated plasmid DNA in aquatic environments. Environ. Toxicol. Water Qual. 11: 129135 3.0.CO;2-B>CrossRef
Andersen, JT, Schafer, T, Jørgensen, PL, Møller, S (2001) Using inactivated microbial biomass as fertilizer: the fate of antibiotic resistance genes in the environment. Res. Microbiol. 152: 823833 CrossRef
Arumuganathan, K, Earle, ED (1991) Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9: 208218 CrossRef
Austin JJ, Smith AB, Thomas RH (1997) Palaeontology in a molecular world: the search for authentic ancient DNA. Trends Ecol. Evol. 12: 303–306
Baker, RT (1977) Humic acid-associated organic phosphate. New Zealand J. Sci. 20: 43941
Battista, JR (1997) Against all odds: the survival strategies of Deinococcus radiodurans. Annu. Rev. Microbiol. 51: 203224 CrossRef
Bauer, T, Weller, P, Hammes, WP, Hertel, C (2003) The effect of processing parameters on DNA degradation in food. Eur. Food Res. Technol. 217: 338343 CrossRef
Bazelyan, VL, Ayzatullin, TA (1979) Kinetics of enzymatic hydrolysis of DNA in sea water. Oceanology 19: 3033
Beebee, TJC (1993) Identification and analysis of nucleic acids in natural freshwaters. Sci. Total Environ. 135: 123129 CrossRef
Beliaeva, MI, Kapranova, MN, Vitol, MI, Golubenko, IA, Leshchinskaia, IB (1976) Nucleic acids utilized as the main source of bacterial nutrition. Mikrobiologica 45: 420424
Benedik, MJ, Strych, U (1998) Serratia marcescens and its extracellular nuclease. FEMS Microbiol. Lett. 165: 113 CrossRef
Bensasson, D, Boore, JL, Nielsen, KM (2004) Genes without frontiers. Heredity 92: 483489 CrossRef
Bergthorsson, U, Adams, KL, Thomason, B, Palmer, JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197201 CrossRef
Bertolla, F, Frostegård, A, Brito, B, Nesme, X, Simonet, P (1999) During infection of its hosts, the plant pathogen Ralstonia solanacearum naturally develops a state of competence and exchanges genetic material. Mol. Plant Microb. Interact. 12: 467472 CrossRef
Bertolla, F, Pepin, R, Passelegue-Robe, E, Paget, E, Simkon, 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: 41614167 CrossRef
Blum, SAE, Lorenz, MG , Wackernagel W (1997) Mechanism of retarded DNA degradation and prokaryotic origin of DNases in nonsterile soil. System. Appl. Microbiol. 20: 513521 CrossRef
Boehme, J, Frischer, ME, Jiang, SC, Kellogg, CA, Pichard, S, Rose, JB, Steinway, C, Paul, JH (1993) Viruses, bacterioplankton, and phytoplankton in the southeastern Gulf of Mexico: distribution and contribution to oceanic DNA pools. Mar. Ecol. Prog. Ser. 97: 110 CrossRef
Borneman, J, Hartin, RJ (2000) PCR primers that amplify fungal rRNA genes from environmental samples. Appl. Environ. Microbiol. 66: 4356–4360 CrossRef
Burns, RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol. Biochem. 14: 423427 CrossRef
Carlson, CA, Pierson, LS, Rosen, JJ, Ingraham, JL (1983) Pseudomonas stutzeri and related species undergo natural transformation. J. Bacteriol. 153: 9399
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: 673678 CrossRef
Chiter, A, Forbes, JM, Blair, GE (2000) DNA stability in plant tissues: implications for the possible transfer of genes from genetically modified food. FEBS Lett. 481: 164168 CrossRef
Cohan, FM, Roberts, MS, King, EC (1991) The potential for genetic exchange by transformation within a natural population of Bacillus subtilis. Evolution 45: 13831421 CrossRef
Coleman, GS (1980) Rumen ciliate protozoa. Adv. Parasitol. 18: 121173 CrossRef
Corinaldesi, C, Danavaro, R, Dell'Anno A (2005) Simultaneous recovery of extracellular and intracellular DNA suitable for molecular studies from marine sediments. Appl. Environ. Microbiol. 71: 4650 CrossRef
Couteaux, MM, Sarmiento, L, Bottner, P, Acevedo, D, Thiery, JM (2002) Decomposition of standard plant material along an altitudinal transect (65-3968 m) in the tropical Andes. Soil Biol. Biochem. 34: 6978 CrossRef
Cuatrecasas, P, Wilcheck, M, Anfinsen, CB (1969) The action of staphylococcal nuclease on synthetic substrates. Biochemistry 8: 22772284 CrossRef
Daniel, R (2005) The metagenomics of soil. Nature Rev. Microbiol. 3: 470478 CrossRef
Daniell, H (1999) New tools for chloroplast genetic engineering. Nature Biotechnol. 17: 855–856 CrossRef
Deere, D, Porter, J, Pickup, RW, Edwards, C (1996) Survival of cells and DNA of Aeromonas salmonicida released into aquatic microcosms. J. Appl. Bacteriol. 81: 309318 CrossRef
DeFlaun, MF, Paul, JH (1989) Detection of exogenous gene sequences in dissolved DNA from aquatic environments. Microb. Ecol. 18: 2128 CrossRef
DeFlaun, MF, Paul, JH, Davis, D (1986) Simplified method for dissolved DNA determination in aquatic environments. Appl. Environ. Microbiol. 52: 654659
DeFlaun, MF, Paul, JH, Jeffrey, WH (1987) Distribution and molecular weight of dissolved DNA in subtropical estuarine and oceanic environments. Mar. Ecol. Prog. Ser. 38: 6573 CrossRef
Degand I, Laporte J, Pussemier L (2002) Monitoring the persistence of genes deriving from genetically modified plants in the soil environment. Meded. Rijksuniv. Gent. Fak. Landbouwkd. Toegep. Biol. Wet. 67: 85–98
Dell'Anno, A, Corinaldesi, C (2004) Degradation and turnover of extracellular DNA in marine sediments: Ecological and methodological considerations. Appl. Environ. Microbiol. 70: 43844386 CrossRef
Dell'Anno, A, Danovaro, R (2005) Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science 309: 2179 CrossRef
Dell'Anno, A, Bompadre, S, Danovaro, R (2002) Quantification, base composition, and fate of extracellular DNA in marine sediments. Limnol. Oceanogr. 47: 899905 CrossRef
Demanèche, S, Jocteur-Monrozier, L, Quiquampoix, H, Simonet, P (2001) Evaluation of biological and physical protection against nuclease degradation of clay-bound plasmid DNA. Appl. Environ. Microbiol. 67: 293299 CrossRef
Desai, NA, Shankar, V (2003) Single strand specific nucleases. FEMS Microbiol. Rev. 26: 457491 CrossRef
DeSalle, R, Gatesy, J, Wheeler, W, Grimaldi, D (1992) DNA sequences from a fossil termite in oligo-miocene amber and their phylogenetic implications. Science 257: 19331936 CrossRef
Dillard, JP, Seifert, HS (2001) A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for genetic transformation and is found more often in disseminated infection isolates. Mol. Microbiol. 41: 263277 CrossRef
Doblhoff-Dier, O, Bachmayer, H, Bennett, A, Brunius, G, Burki, K, Cantley, M, Collins, C, Crooy, P, Elmqvist, A, Frontali-Botti, C, Havenaar, R, Haymerle, H, Lelieveld, H, Lex, M, Mahler, JL, Martinez, L, Mosgaard, C, Olsen, L, Pazlarova, J, Rudan, F, Sarvas, M, Stepankova, H, Tzotzos, G, Wagner, K, Werner, R (2000) DNA content of biotechnological process waste. Trends Biotechnol. 18: 141146
Douville, M, Gagne, F, Blaise, C, Andre, C (2007) Occurrence and persistence of Bacillus thuringiensis (Bt) and transgenic Bt corn cry1Ab gene from an aquatic environment. Ecotoxicol. Environ. Safety 66: 195203 CrossRef
Dupray, E, Caprais, MP, Derrien, A, Fach, P (1997) Salmonella DNA persistence in natural seawaters using PCR analysis. J. Appl. Microbiol. 82: 507510 CrossRef
Eaves, GN, Jeffries, CD (1963) Isolation and properties of an extracellular nuclease of Serratia marcescens. J. Bacteriol. 85: 273278
England, LS, Lee, H, Trevors, JT (1997) Persistence of Pseudomonas aureofaciens strains and DNA in soil. Soil Biol. Biochem. 29: 15211527 CrossRef
England, LS, Pollok, J, Vincent, M, Kreutzweiser, D, Fick, W, Trevors, JT, Holmes, SB (2005) Persistence of extracellular baculoviral DNA in aquatic microcosms: extraction, purification, and amplification by the polymerase chain reaction (PCR). Mol. Cell. Probes 19: 7580 CrossRef
Feil, EJ, Spratt, BG (2001) Recombination and the population structure of bacterial pathogens. Annu. Rev. Microbiol. 55: 561590 CrossRef
Finkel, SE, Kolter, R (2001) DNA as a nutrient: novel role for bacterial competence gene homologs. J. Bacteriol. 183: 62886293 CrossRef
Friedlander, AM (1975) DNA release as a direct measure of microbial killing. I. Serum bactericidal activity. J. Immunol. 115: 14041408
Frostegård, Å, Courtois, S, Ramisse, V, Clerc, S, Bernillon, D, Le Gall, F, Jeannin, P, Nesme, X, Simonet, P (1999) Quantification of bias related to the extraction of DNA directly from soils. Appl. Environ. Microbiol. 65: 54095420
Gallori, E, Bazzicalupo, M, Dal Canto, L, Fani, R, Nannipieri, P, Vettori, C, Stotzky, G (1994) Transformation of Bacillus subtilis by DNA bound on clay in non-sterile soil. FEMS Microbiol. Ecol. 15: 119126 CrossRef
Garces, H, Durzan, D, Pedroso, MC (2001) Mechanical stress elicits nitric oxide formation and DNA fragmentation in Arabidopsis thaliana. Ann. Bot. 87: 567574 CrossRef
Gavrieli, Y, Sherman, Y, Ben-Sasson, SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119: 493501 CrossRef
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: 261272 CrossRef
Graham, JB, Istock, CA (1979) Gene exchange and natural selection cause Bacillus subtilis to evolve in soil culture. Science 204: 637639 CrossRef
Graham, JB, Istock, CA (1978) Genetic exchange in Bacillus subtilis in soil. Mol. Gen. Genet. 166: 287290
Greaves, MP, Wilson, MJ (1969) The adsorption of nucleic acids by montmorillonite. Soil Biol. Biochem. 1: 317323 CrossRef
Green, PJ (1994) The ribonucleases of higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 421445 CrossRef
Grimont F, Grimont PAD (1991) The genus Serratia. In Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH, eds, The prokaryotes, Springer Verlag, New York, pp 2822–2849
Guan J, Spencer JL, Ma BL (2005) The fate of recombinant DNA in corn during composting. J. Environ. Sci. Health. Part B. 40: 463–473
Hamilton, HL, Dominguez, NM, Schwartz, KJ, Hackett, KT, Dillard, JP (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55: 17041721 CrossRef
Harter, RD, Stotzky, G (1971) Formation of clay-protein complexes. Soil. Sci. Soc. Amer. Proc. 35: 383389 CrossRef
Havel, L, Durzan, DJ (1996) Apoptosis in plants. Botanica Acta 109: 110 CrossRef
Hay, I, Morency, MJ, Sequin, A (2002) Assessing the persistence of DNA in decomposing leaves of genetically modified poplar trees. Can. J. For. Res. 32: 977982 CrossRef
Henschke, RB, Henschke, EJ, Schmidt, FRJ (1991) Monitoring survival and gene transfer in soil microcosms of recombinant Escherichia coli designed to represent an industrial production strain. Appl. Microbiol. Biotechnol. 35: 247252 CrossRef
Hofreiter, M, Serre, D, Poinar, HN, Kuch, M, Paabo, S (2001) Ancient DNA. Nature Genet. 2: 353359 CrossRef
Huang, CY, Aycliffe, MA, Timmis, JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422: 7276 CrossRef
Iudica, CA, Whitten, W, Williams, NH (2001) Small bones from dried mammal museum specimens as a reliable source of DNA. BioTechniques 30: 732736
Jiang, SC, Paul, JH (1995) Viral contribution to dissolved DNA in the marine kingdom as determined by differential centrifugation and kingdom probing. Appl. Environ. Microbiol. 61: 317325
Jørgensen, NOG, Jacobsen, CS (1996) Bacterial uptake and utilization of dissolved DNA. Aquat. Microb. Ecol. 11: 263270 CrossRef
Kahn, MS, Maliga, P (1999) Fluorescent antibiotic resistance marker for tracking plastid transformation in higher plants. Nature Biotechnol. 17: 910915 CrossRef
Karl, DM, Bailiff, MD (1989) The measurement and distribution of dissolved nucleic acids in aquatic environments. Limnol. Oceanogr. 34: 543558 CrossRef
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: 33453351 CrossRef
Kim, CK, Kwak, MJ, Lee, SG (1996) Structural and functional stability of the genetic recombinant plasmid pCU103 in different water environments. J. Microbiol. 34: 241247
Kögel-Knabner, I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol. Biochem. 32: 139162 CrossRef
Krause, DO, Smith, WJ, McSweeney, CS (2001) Extraction of microbial DNA from rumen contents containing plant tannins. BioTechniques 31: 294298
Ladd JN (1978) Origin and range of enzymes in soil. In Burns RG, ed, Soil Enzymes, Academic Press, London, pp 51–97
Ladd JN, Forster RC, Nannipieri P, Oades JM (1996) Soil structure and biological activity. In Stotzky G, Bollag J-M, eds, Soil Structure and Biological Activity, Marcel Dekker, New York, pp 23–78
Landweber L (1999) Something old for something new: The future of ancient DNA in conservation biology. In Landweber L, Dobson AP, eds, Genetics and the extinction of species: DNA and the conservation of biodiversity, Princeton University Press, New Jersey, USA, pp 163–186
Lee, GH, Stotzky, G (1990) Transformation is a mechanism of gene transfer in soil. Kor. J. Microbiol. 28: 210218
Lee, GH, Stotzky, G (1999) Transformation and survival of donor, recipient, and transformants of Bacillus subtilis in vitro and in soil. Soil Biol. Biochem. 31: 14991508 CrossRef
Lindahl, V, Bakken, LR (1995) Evaluation of methods for extraction of bacteria from soil. FEMS Microbiol. Ecol. 16: 135142 CrossRef
Lorenz MG, Wackernagel W (1987) Adsorption of DNA to sand and variable degradation rates of adsorbed DNA. Appl. Environ. Microbiol. 53: 2948–2952
Lorenz, MG, Wackernagel, W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58: 563602
Lorenz, MG, Aardema, BW, Krumbein, WE (1981) Interaction of marine sediment with DNA and DNA availability to nucleases. Mar. Biol. 64: 225230 CrossRef
Lorenz, MG, Gerjets, D, Wackernagel, W (1991) Release of transforming plasmid and chromosomal DNA from two cultured soil bacteria. Arch. Microbiol. 156: 319326 CrossRef
Luna, GM, Dell'Anno, A, Danovaro, R (2006) DNA extraction procedure: a critical issue for bacterial diversity assessment in marine sediments. Environ. Microbiol. 8: 308320 CrossRef
Lynch JM (1983) Soil Biotechnology. Blackwell Scientific Publications, Oxford, London, pp 42–59
Maeda, M, Taga, N (1973) Deoxyribonuclease activity in seawater and sediment. Mar. Biol. 20: 5863 CrossRef
Maeda, M, Taga, N (1974) Occurrence and distribution of deoxyribonucleic acid-hydrolyzing bacteria in seawater. J. Exp. Mar. Biol. Ecol. 14: 157169 CrossRef
Martin-Laurent, F, Phillipot, L, Hallet, S, Chaussod, R, Germon, JC, Soulas, G, Catroux, G (2001) DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl. Environ. Microbiol. 67: 23542359 CrossRef
Matsui, K, Honjo, M, Kawabata, Z (2001) Estimation of the fate of dissolved DNA in thermally stratified lake water from the stability of exogenous plasmid DNA. Aquat. Microb. Ecol. 26: 95102 CrossRef
Matsui, K, Ishii, N, Kawabata, Z (2003) Release of extracellular transformable plasmid DNA from Escherichia coli cocultivated with algae. Appl. Environ. Microbiol. 69: 23992404 CrossRef
Maynard Smith, J, Feil, EJ, Smith, NH (2000) Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 22: 11151122 3.0.CO;2-R>CrossRef
Minear, RA (1972) Characterization of naturally occurring dissolved organophosphorus compounds. Environ. Sci. Technol. 6: 431437 CrossRef
Miraglia, M, Berdal, KG, Brera, C, Corbisier, P, Holst-Jensen, A, Kok, EJ, Marvin, HJ, Schimmel, H, Rentsch, J, van Rie, JP, Zagon, J (2004) Detection and traceability of genetically modified organisms in the food production chain. Food Chem. Toxicol. 42: 11571180 CrossRef
Muela, A, Arana, I, Justo, JI, Seco, C, Barcina, I (1999) Changes in DNA content and cellular death during a starvation-survival process of Escherichia coli in river water. Microb. Ecol. 37: 6269 CrossRef
Nagata, S (2005) DNA degradation in development and programmed cell death. Ann. Rev. Immunol. 23: 853875 CrossRef
Nannipieri P (1994) The potential use of soil enzymes as indicators of productivity, sustainability and pollution. In Pankhurst CE, Doube BM, Gupta VVSR, Grace PR, eds, Soil biota, CSIRO, Adelaide, Australia, pp 238–244
Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In Burns RG, Dick R, eds, Enzymes in the Environment: Activity, Ecology, and Applications, Marcel Dekker, New York, pp 1–33
Nielsen KM, Townsend JP (2004) Monitoring and modeling horizontal gene transfer. Nature Biotechnol. 22: 1110–1114
Nielsen KM, van Weerelt MDM, Berg TN, Bones AM, Hagler AN, van Elsas JD (1997a) Natural transformation and availability of transforming DNA to Acinetobacter calcoaceticus in soil microcosms. Appl. Environ. Microbiol. 63: 1945–1952
Nielsen KM, Bones AM, van Elsas JD (1997b) Induced natural transformation of Acinetobacter calcoaceticus in soil microcosms. Appl. Environ. Microbiol. 63: 3972–3977
Nielsen KM, Smalla K, van Elsas JD (2000) Natural transformation of Acinetobacter sp. strain BD413 with cell lysates of Acinetobacter sp., Pseudomonas fluorescens and Burkholderia cepacia in soil microcosms. Appl. Environ. Microbiol. 66: 206–212
Nielsen KM, van Elsas JD, Smalla K (2001) Dynamics, horizontal transfer and selection of novel DNA in the phytosphere of transgenic plants. Ann. Microbiol. 51: 79–94
Nielsen KM, Calamai L, Pietramellara G (2006) Stabilization of extracellular DNA and proteins by transient binding to various soil components. In Nannipieri P, Smalla K, eds, Soil Biology, Vol. 8, Nucleic acids and proteins in soil, Springer Verlag, Heidelberg, Germany, pp 141–157
Nielsen KM, Johnsen P, van Elsas JD (2007) Gene transfer and micro-evolution in soil. In van Elsas JD, Janssen JK, Trevors J, eds, Modern Soil Microbiology, 2nd edn, CRC Press, pp 55–81
Niemeyer J, Gessler F (2002) Determination of free DNA in soils. J. Plant Nutr. Soil Sci. 165: 121–124
Novitsky JA (1986) Degradation of dead microbial biomass in a marine sediment. Appl. Environ. Microbiol. 52: 504–509
Nygaard I (1983) Utilization of preformed purine bases and nucleosides. In Munch-Pedersen A, ed, Metabolism of nucleosides and nucleobases in microorganisms, Academic press, London, pp 27–93
Oades, JM (1988) The retention of organic matter in soils. Biogeochemistry 5: 3570 CrossRef
Ogram, A, Sayler, GS, Barkay, T (1987) The extraction and purification of microbial DNA from sediments. J. Microbiol. Meth. 7: 5766 CrossRef
Paget, E, Simonet, P (1994) On the track of natural transformation in soil. FEMS Microbiol. Ecol. 15: 109118 CrossRef
Paget E, Lebrun M, Freyssinet G, Simonet P (1998) The fate of recombinant plant DNA in soil. Eur. J. Soil Biol. 34: 81–88
Palmen R, Hellingwerf KJ (1995) Acinetobacter calcoaceticus liberates chromosomal DNA during induction of competence by cell lysis. Curr. Microbiol. 30: 7–10
Palmen R, Hellingwerf KJ (1997) Uptake and processing of DNA by Acinetobacter calcoaceticus – a review. Gene 192: 179–190
Palmer, CJ, Tsai, YL, Paszko-Kolva, C, Mayer, C, Sangeramo, LR (1993) Detection of Legionella species in sewage and ocean water by polymerase chain reaction, direct fluorescent-antibody, and plate culture methods. Appl. Environ. Microbiol. 59: 36183624
Paul, JH, Myers, B (1982) Fluorometric determination of DNA in aquatic microorganisms by use of Hoechst 33258. Appl. Environ. Microbiol. 43: 13931399
Paul JH, Jeffrey WH, DeFlaun MF (1987) Dynamics of extracellular DNA in the marine environment. Appl. Environ. Microbiol. 53: 170–179
Paul JH, Jeffrey WH, David AW, DeFlaun MF, Cazares LH (1989) Turnover of extracellular DNA in eutrophic and oligotrophic environments of southwest Florida. Appl. Environ. Microbiol. 55: 1823–1828
Paul JH, Jeffrey WH, Cannon JP (1990) Production of dissolved DNA, RNA, and protein by microbial populations in a Florida reservoir. Appl. Environ. Microbiol. 56: 2957–2962
Pettersen, AK, Primicero, R, Bøhn, T, Nielsen, KM (2005) Modeling suggest frequency estimates are not informative for predicting the long-term effect of horizontal gene transfer in bacteria. Environ. Biosafety Res. 4: 222233
Pietramellara, G, Canto, L, Vettori, C, Gallori, E, Nannipieri P (1997) Effects of air-drying and wetting cycles on the transforming abiliting of DNA bound on clay minerals. Soil Biol. Biochem. 29: 5561 CrossRef
Pillai, TVN, Ganguly, AK (1970) Nucleic acids in the dissolved constituents of seawater. Curr. Sci. 22: 501504
Pillai TVN, Ganguly AK (1972) Nucleic acids in the dissolved constituents of seawater. J. Mar. Biol. Ass. India 14: 384–390
Puyet, A, Greenberg, B, Lacks, SA (1990) Genetic and structural characterization of endA. A membrane-bound nuclease required for transformation of Streptococcus pneumoniae. J. Mol. Biol. 213: 727738 CrossRef
Rangarajan, ES, Shankar, V (2001) Sugar non-specific endonucleases. FEMS. Microb. Rev. 25: 583613 CrossRef
Recorbet G, Picard C, Normand P, Simonet P (1993) Kinetics of persistence of chromosomal DNA from genetically engineered Escherichia coli introduced into soil. Appl. Environ. Microbiol. 59: 4289–4294
Ricchetti, M, Fairhead, C, Dujon, B (1999) Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402: 96100 CrossRef
Richards BN (1987) Microbiology of the rhizosphere. Longman Science & Technology, Essex, England, pp 222–254
Rizzi, AL, Panebianco, D, Giacca, Sorlini, C, Daffonchio, D (2003) Stability and recovery of maize DNA during food processing. Italian J. Food Sci. 15: 499510
Robe P, Nalin R, Capellano C, Vogel TM, Simonet P (2003) Extraction of DNA from soil. Eur. J. Soil Biol. 39: 183–190
Romanowski G, Lorenz MG, Sayler G, Wackernagel W (1992) Persistence of free plasmid DNA in soil monitored by various methods, including a transformation assay. Appl. Environ. Microbiol. 58: 3012–3019
Romanowski, G, Lorenz, MG, Wackernagel, W (1993) Plasmid DNA in a groundwater aquifer microcosm – adsorption, DNase resistance and natural genetic transformation of Bacillus subtilis. Mol. Ecol. 2: 171181 CrossRef
Ruiz, TR, Andrews, S, Smith, GB (2000) Identification and characterization of nuclease activities in anaerobic environmental samples. Can. J. Microbiology 46: 736740 CrossRef
Ryerson, DE, Heath, MC (1996) Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8: 393402 CrossRef
Saano, A, Kajialainen, S, Lindstrom, K (1993) Inhibition of DNA mobilization to nylon membrane by soil compounds. Microb. Releases 2: 153160
Selenska, S, Klingmüller, W (1991) DNA recovery and direct detection of Tn5 sequences from soil. Lett. Appl. Microbiol. 13: 2124 CrossRef
Selenska S, Klingmüller W (1992) Direct recovery and molecular analysis of DNA and RNA from soil. Microb. Releases 1: 41–46
Sikorski J, Graupner S, Lorenz MG, Wackernagel W (1998) Natural genetic transformation of Pseudomonas stutzeri in a non-sterile soil. Microbiology 144: 569–76
Siuda, W, Gude, H (1996) Determination of dissolved deoxyribonucleic acid concentration in lake water. Aquat. Microb. Ecol. 11: 193202 CrossRef
Smit E, Leeflang P, Glandorf B, van Elsas JD, Wernars K (1999) Analysis of fungal diversity on the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl. Environ. Microbiol. 65: 2614–2621
Steinberger RE, Holden PA (2005) Extracellular DNA in single-and multiple-species unsaturated biofilms. Appl. Environ. Microbiol. 71: 5404–5410
Stewart, GJ, Sinigalliano, CD, Garko, KA (1991) Binding of exogenous DNA to marine sediments and the effect of DNA/sediment binding on natural transformation of Pseudomonas stutzeri strain Zobell in sediment columns. FEMS Microbiol. Ecol. 85: 18 CrossRef
Tebbe CC, Vahjen W (1993) Interference of humic acids and DNA extracted directly from soil in detection and transformation of recombinant DNA from bacteria and a yeast. Appl. Environ. Microbiol. 59: 2657–2665
Thomas, CM, Nielsen, KM (2005) Mechanisms and barriers to horizontal gene transfer between bacteria. Nature Rev. Microbiol. 3: 711721 CrossRef
Thomas, H, Stoddart, J (1980) Leaf senescence. Annu. Rev. Plant Physiol. 31: 83111 CrossRef
Thorsness PE, White KH, Fox D (1993) Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 5418–5426
Torsvik, VL, Goksøyr, J (1978) Determination of bacterial DNA in soil. Soil Biol. Biochem. 10: 712 CrossRef
Torsvik V, Goksøyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl. Environ. Microbiol. 56: 782–787
Trevors JT, van Elsas JD, eds (1995) Nucleic acids in the environment, Springer Verlag, Berlin-Heidelberg
Tsai YL, Olson BH (1992) Detection of low numbers of bacterial cells in soils and sediments by polymerase chain reaction. Appl. Environ. Microbiol. 58: 754–757
Turk, V, Rehnstam, AS, Lundberg, E, Hagstrøm Å (1992) Release of bacterial DNA by marine nanoflagellates, an intermediate step in phosphorous regeneration. Appl. Environ. Microbiol. 58: 37443750
van Elsas JD, Duarte GF, Keijzer-Wolters A, Smit E (2000) Analysis of the dynamics of fungal communities in soil via fungal-specific PCR of soil DNA followed by denaturing gradient gel electrophoresis. J. Microbiol. Meth. 43: 133–151
Vaneechoutte M, Young DM, Ornston LN, De Baere T, Nemec A, Van Der Reijden T, Carr E, Tjernberg I, Dijkshoorn L (2006) Naturally transformable Acinetobacter sp. strain ADP1 belongs to the newly described species Acinetobacter baylyi. Appl. Environ. Microbiol. 72: 932–936
Vincent, RD, Hofmann, TT, Zassenhaus, HP (1988) Sequence and expression of NUC1, the gene encoding the mitochondrial nuclease in Saccharomyces cerevisiae. Nucleic Acids Res. 16: 32973312 CrossRef
Whitchurch, CB, Tolker-Nielsen, T, Ragas, PC, Mattick, JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1497 CrossRef
White, O, Eisen, JA, Heidelberg, JF, Hickey, EK, Peterson, JD, Dodson, RJ, Haft, DH, Gwinn, ML, Nelson, WC, Richardson, DL, Moffat, KS, Qin, H, Jiang, L, Pamphile, W, Crosby, M, Shen, M, Vamathevan, JJ, Lam, P, McDonald, L, Utterback, T, Zalewski, C, Makarova, KS, Aravind, L, Daly, MJ, Minton, KW, Fleischmann, RD, Ketchum, KA, Nelson, KE, Salzberg, S, Smith, HO, Venter, JC, Fraser, CM (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286: 15711577 CrossRef
Widmer, F, Seidler, RJ, Watrud, LS (1996) Sensitive detection of transgenic plant marker gene persistence in soil microcosms. Mol. Ecol. 5: 603613 CrossRef
Widmer, F, Seidler, RJ, Donegan, KK, Reed, GL (1997) Quantification of transgenic plant marker gene persistence in the field. Mol. Ecol. 6: 17 CrossRef
Woodhouse HW (1982) Leaf senescence. In Smith H, Grierson D, eds, The molecular biology of plant development, Blackwell, Oxford, pp 256–281
Yin X, Stotzky G (1997) Gene transfer among bacteria in natural environments. Adv. Appl. Microbiol. 45: 153–212
Yonemura, K, Matsumoto, K, Maeda, H (1983) Isolation and characterization of nucleases from a clinical isolate of Serratia marcescens kums 3958. J. Biochem. 93: 12871295 CrossRef
Yu X, Gabriel A (1999) Patching broken chromosomes with extranuclear cellular DNA. Mol. Cell. 4: 873–881
Zawadzki, P, Cohan, FM (1995) The size and continuity of DNA segments integrated in Bacillus transformation. Genetics 141: 12311243
Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62: 316–322
Zweifel UL, Hagstrøm A (1995) Total counts of marine bacteria include a large fraction of nun-nucleoid-containing bacteria (ghosts). Appl. Environ. Microbiol. 61: 2180–2185