Release and persistence of extracellular DNA in the environment.

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.

[1]  Z. Kawabata,et al.  Release of Extracellular Transformable Plasmid DNA from Escherichia coli Cocultivated with Algae , 2003, Applied and Environmental Microbiology.

[2]  G. B. Smith,et al.  Identification and characterization of nuclease activities in anaerobic environmental samples. , 2000, Canadian journal of microbiology.

[3]  Paul R Shorten,et al.  Modeling suggests frequency estimates are not informative for predicting the long-term effect of horizontal gene transfer in bacteria. , 2005, Environmental biosafety research.

[4]  Christopher M Thomas,et al.  Mechanisms of, and Barriers to, Horizontal Gene Transfer between Bacteria , 2005, Nature Reviews Microbiology.

[5]  Å. Hagström,et al.  Total counts of marine bacteria include a large fraction of non-nucleoid-containing bacteria (ghosts) , 1995, Applied and environmental microbiology.

[6]  J. Ingraham,et al.  Pseudomonas stutzeri and related species undergo natural transformation , 1983, Journal of bacteriology.

[7]  J. Novitsky Degradation of Dead Microbial Biomass in a Marine Sediment , 1986, Applied and environmental microbiology.

[8]  H. Nam,et al.  Leaf senescence. , 2007, Annual review of plant biology.

[9]  E. Feil,et al.  Population structure and evolutionary dynamics of pathogenic bacteria , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[10]  Sunny C. Jiang,et al.  Viruses, Bacterioplankton, and Phytoplankton in the Southeastern Gulf of Mexico: Distribution and Contribution to Oceanic DNA Pools , 1993 .

[11]  T. Beebee Identification and analysis of nucleic acids in natural freshwaters , 1993 .

[12]  S. Lacks,et al.  Genetic and structural characterization of endA. A membrane-bound nuclease required for transformation of Streptococcus pneumoniae. , 1990, Journal of molecular biology.

[13]  X. Yu,et al.  Patching broken chromosomes with extranuclear cellular DNA. , 1999, Molecular cell.

[14]  B H Olson,et al.  Detection of low numbers of bacterial cells in soils and sediments by polymerase chain reaction , 1992, Applied and environmental microbiology.

[15]  Mario Vaneechoutte,et al.  Naturally Transformable Acinetobacter sp. Strain ADP1 Belongs to the Newly Described Species Acinetobacter baylyi , 2006, Applied and Environmental Microbiology.

[16]  Y. Tsai,et al.  Detection of Legionella species in sewage and ocean water by polymerase chain reaction, direct fluorescent-antibody, and plate culture methods , 1993, Applied and environmental microbiology.

[17]  P. Simonet,et al.  On the track of natural transformation in soil , 1994 .

[18]  J. P. Dillard,et al.  Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system , 2005, Molecular microbiology.

[19]  Roberto Danovaro,et al.  Simultaneous Recovery of Extracellular and Intracellular DNA Suitable for Molecular Studies from Marine Sediments , 2005, Applied and Environmental Microbiology.

[20]  I. Kögel‐Knabner The Macromolecular Organic Composition of Plant and Microbial Residues as Inputs to Soil Organic Matter. , 2002 .

[21]  S. Nagata DNA degradation in development and programmed cell death. , 2005, Annual review of immunology.

[22]  M. G. Lorenz,et al.  Natural genetic transformation of Pseudomonas stutzeri in a non-sterile soil. , 1998, Microbiology.

[23]  M. G. Lorenz,et al.  Bacterial gene transfer by natural genetic transformation in the environment. , 1994, Microbiological reviews.

[24]  C. McSweeney,et al.  Extraction of microbial DNA from rumen contents containing plant tannins. , 2001, BioTechniques.

[25]  G. Blair,et al.  DNA stability in plant tissues: implications for the possible transfer of genes from genetically modified food , 2000, FEBS letters.

[26]  J. Tiedje,et al.  DNA recovery from soils of diverse composition , 1996, Applied and environmental microbiology.

[27]  I. Arana,et al.  Changes in DNA Content and Cellular Death during a Starvation-Survival Process of Escherichia coli in River Water , 1999, Microbial Ecology.

[28]  J. Paul,et al.  Distribution and Molecular Weight of Dissolved DNA in Subtropical Estuarine and Oceanic Environments , 1987 .

[29]  D. Ryerson,et al.  Cleavage of Nuclear DNA into Oligonucleosomal Fragments during Cell Death Induced by Fungal Infection or by Abiotic Treatments. , 1996, The Plant cell.

[30]  R. Danovaro,et al.  Quantification, base composition, and fate of extracellular DNA in marine sediments , 2002 .

[31]  C. Istock,et al.  Genetic exchange in Bacillus subtilis in soil , 1978, Molecular and General Genetics MGG.

[32]  Chun-Yuan Huang,et al.  Direct measurement of the transfer rate of chloroplast DNA into the nucleus , 2003, Nature.

[33]  H Schimmel,et al.  Detection and traceability of genetically modified organisms in the food production chain. , 2004, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[34]  M. S. Khan,et al.  Fluorescent antibiotic resistance marker for tracking plastid transformation in higher plants , 1999, Nature Biotechnology.

[35]  G. Sayler,et al.  Persistence of Free Plasmid DNA in Soil Monitored by Various Methods, Including a Transformation Assay , 1992, Applied and environmental microbiology.

[36]  X. Nesme,et al.  During infection of its host, the plant pathogen Ralstonia solanacearum naturally develops a state of competence and exchanges genetic material , 1999 .

[37]  P. Green,et al.  The Ribonucleases of Higher Plants , 1994 .

[38]  W. Klingmüller,et al.  Direct recovery and molecular analysis of DNA and RNA from soil. , 1992, Microbial releases : viruses, bacteria, fungi.

[39]  R. Joergensen,et al.  Relationship between simulated spatial variability and some estimates of microbial biomass turnover , 2000 .

[40]  M. G. Lorenz,et al.  Plasmid DNA in a groundwater aquifer microcosm ‐adsorption, DNAase resistance and natural genetic transformation of Bacillus subtilis , 1993, Molecular ecology.

[41]  W. M. Whitten,et al.  Small bones from dried mammal museum specimens as a reliable source of DNA. , 2001, BioTechniques.

[42]  D. Durzan,et al.  Mechanical Stress Elicits Nitric Oxide Formation and DNA Fragmentation in Arabidopsis thaliana , 2001 .

[43]  R. Fani,et al.  Transformation of Bacillus subtilis by DNA bound on clay in non-sterile soil. , 1994 .

[44]  J. Trevors,et al.  Persistence of extracellular baculoviral DNA in aquatic microcosms: extraction, purification, and amplification by the polymerase chain reaction (PCR). , 2005, Molecular and cellular probes.

[45]  R. DeSalle,et al.  DNA sequences from a fossil termite in Oligo-Miocene amber and their phylogenetic implications. , 1992, Science.

[46]  W. Siuda,et al.  Determination of dissolved deoxyribonucleic acid concentration in lake water , 1996 .

[47]  P. Simonet,et al.  Evaluation of Biological and Physical Protection against Nuclease Degradation of Clay-Bound Plasmid DNA , 2001, Applied and Environmental Microbiology.

[48]  J. Paul,et al.  Viral contribution to dissolved DNA in the marine environment as determined by differential centrifugation and kingdom probing , 1995, Applied and environmental microbiology.

[49]  V. Torsvik,et al.  High diversity in DNA of soil bacteria , 1990, Applied and environmental microbiology.

[50]  V. Turk,et al.  Release of Bacterial DNA by Marine Nanoflagellates, an Intermediate Step in Phosphorus Regeneration , 1992, Applied and environmental microbiology.

[51]  K. H. White,et al.  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 , 1993, Molecular and cellular biology.

[52]  C. Sorlini,et al.  Stability and recovery of maize DNA during food processing , 2003 .

[53]  G. Coleman Rumen ciliate protozoa. , 1980, Advances in parasitology.

[54]  J. Battista,et al.  Against all odds: the survival strategies of Deinococcus radiodurans. , 1997, Annual review of microbiology.

[55]  C. Anfinsen,et al.  The action of staphylococcal nuclease on synthetic substrates. , 1969, Biochemistry.

[56]  F. Grimont,et al.  The genus Serratia. , 1978, Annual review of microbiology.

[57]  R. Minear Characterization of naturally occurring dissolved organophosphorus compounds , 1972 .

[58]  D. Karl,et al.  The measurement and distribution of dissolved nucleic acids in aquatic environments , 1989 .

[59]  A. Friedlander DNA release as a direct measure of microbial killing. I. Serum bactericidal activity. , 1975, Journal of Immunology.

[60]  V. Torsvik,et al.  Determination of bacterial DNA in soil , 1978 .

[61]  G. Stotzky,et al.  Transformation and survival of donor, recipient, and transformants of Bacillus subtilis in vitro and in soil , 1999 .

[62]  J. Trevors,et al.  Persistence of Pseudomonas aureofaciens strains and DNA in soil , 1997 .

[63]  S. Salzberg,et al.  Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. , 1999, Science.

[64]  J. Mattick,et al.  Extracellular DNA required for bacterial biofilm formation. , 2002, Science.

[65]  S. Gite,et al.  Single-strand-specific nucleases. , 1995, Critical reviews in microbiology.

[66]  J. Paul,et al.  Simplified Method for Dissolved DNA Determination in Aquatic Environments , 1986, Applied and environmental microbiology.

[67]  R. Kolter,et al.  DNA as a Nutrient: Novel Role for Bacterial Competence Gene Homologs , 2001, Journal of bacteriology.

[68]  G. Soulas,et al.  DNA Extraction from Soils: Old Bias for New Microbial Diversity Analysis Methods , 2001, Applied and Environmental Microbiology.

[69]  S. Pääbo,et al.  Ancient DNA , 2001, Nature Reviews Genetics.

[70]  H. Seifert,et al.  A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates , 2001, Molecular microbiology.

[71]  Jeffrey D. Palmer,et al.  Widespread horizontal transfer of mitochondrial genes in flowering plants , 2003, Nature.

[72]  J. Boore,et al.  Genes without frontiers? , 2004, Heredity.

[73]  C. Jacobsen,et al.  Bacterial uptake and utilization of dissolved DNA , 1996 .

[74]  E. Gallori,et al.  Effects of air-drying and wetting cycles on the transforming ability of DNA bound on clay minerals , 1997 .

[75]  J. Paul,et al.  Turnover of Extracellular DNA in Eutrophic and Oligotrophic Freshwater Environments of Southwest Florida , 1989, Applied and environmental microbiology.

[76]  J. Niemeyer,et al.  Determination of free DNA in soils , 2002 .

[77]  T. Vogel,et al.  In Situ Transfer of Antibiotic Resistance Genes from Transgenic (Transplastomic) Tobacco Plants to Bacteria , 2002, Applied and Environmental Microbiology.

[78]  M. G. Lorenz,et al.  Release of transforming plasmid and chromosomal DNA from two cultured soil bacteria , 2004, Archives of Microbiology.

[79]  M. P. Greaves,et al.  The adsorption of nucleic acids by montmorillonite , 1969 .

[80]  Henry Daniell,et al.  New tools for chloroplast genetic engineering , 1999, Nature Biotechnology.

[81]  L. Pussemier,et al.  Monitoring the persistence of genes deriving from genetically modified plants in the soil environment. , 2002, Mededelingen.

[82]  J. Paul,et al.  Fluorometric determination of DNA in aquatic microorganisms by use of hoechst 33258. , 1982, Applied and environmental microbiology.

[83]  K. Smalla,et al.  Monitoring field releases of genetically modified sugar beets for persistence of transgenic plant DNA and horizontal gene transfer , 1999 .

[84]  P. Nannipieri,et al.  Soil structure and biological activity , 1996 .

[85]  H. Maeda,et al.  Isolation and characterization of nucleases from a clinical isolate of Serratia marcescens kums 3958. , 1983, Journal of Biochemistry (Tokyo).

[86]  Chi-Kyung Kim,et al.  Structural and Functional Stability of the Genetic Recombinant Plasmid pCU103 in Different Water Environments , 1996 .

[87]  G. Toranzos,et al.  Stability of manipulated plasmid DNA in aquatic environments , 1996 .

[88]  R. Danovaro,et al.  Extracellular DNA Plays a Key Role in Deep-Sea Ecosystem Functioning , 2005, Science.

[89]  K. Nielsen,et al.  Dynamics, horizontal transfer and selection of novel DNA in bacterial populations in the phytosphere of transgenic plants , 2001 .

[90]  L. Havel,et al.  Apoptosis in plants , 1996 .

[91]  K. Nielsen,et al.  Natural Transformation of Acinetobactersp. Strain BD413 with Cell Lysates of Acinetobacter sp.,Pseudomonas fluorescens, and Burkholderia cepaciain Soil Microcosms , 2000, Applied and Environmental Microbiology.

[92]  L. Bakken,et al.  Evaluation of methods for extraction of bacteria from soil , 1995 .

[93]  R. B. Henschke,et al.  Monitoring survival and gene transfer in soil microcosms of recombinant Escherichia coli designed to represent an industrial production strain , 1991, Applied Microbiology and Biotechnology.

[94]  R. J. Hartin,et al.  PCR Primers That Amplify Fungal rRNA Genes from Environmental Samples , 2000, Applied and Environmental Microbiology.

[95]  J. Paul,et al.  Production of dissolved DNA, RNA, and protein by microbial populations in a Florida reservoir , 1990, Applied and environmental microbiology.

[96]  M. G. Lorenz,et al.  The extracellular nuclease of Serratia marcescens: studies on the activity in vitro and effect on transforming DNA in a groundwater aquifer microcosm , 2004, Archives of Microbiology.

[97]  V. Ramisse,et al.  Quantification of Bias Related to the Extraction of DNA Directly from Soils , 1999, Applied and Environmental Microbiology.

[98]  M. Roberts,et al.  THE POTENTIAL FOR GENETIC EXCHANGE BY TRANSFORMATION WITHIN A NATURAL POPULATION OF BACILLUS SUBTILIS , 1991, Evolution; international journal of organic evolution.

[99]  P. Bottner,et al.  Decomposition of standard plant material along an altitudinal transect (65–3968m) in the tropical Andes , 2002 .

[100]  F. Cohan,et al.  The size and continuity of DNA segments integrated in Bacillus transformation. , 1995, Genetics.

[101]  B. Ma,et al.  The Fate of the Recombinant DNA in Corn During Composting , 2005, Journal of environmental science and health. Part. B, Pesticides, food contaminants, and agricultural wastes.

[102]  R. H. Thomas,et al.  Palaeontology in a molecular world: the search for authentic ancient DNA. , 1997, Trends in ecology & evolution.

[103]  P. Simonet,et al.  The fate of recombinant plant DNA in soil , 1998 .

[104]  J. Trevors Nucleic Acids in the Environment , 1995, Springer Lab Manuals.

[105]  P. Holden,et al.  Extracellular DNA in Single- and Multiple-Species Unsaturated Biofilms , 2005, Applied and Environmental Microbiology.

[106]  G. M. Luna,et al.  DNA extraction procedure: a critical issue for bacterial diversity assessment in marine sediments. , 2006, Environmental microbiology.

[107]  L. Watrud,et al.  Sensitive detection of transgenic plant marker gene persistence in soil microcosms , 1996 .

[108]  W. Vahjen,et al.  Interference of humic acids and DNA extracted directly from soil in detection and transformation of recombinant DNA from bacteria and a yeast , 1993, Applied and environmental microbiology.

[109]  J. Paul,et al.  Detection of exogenous gene sequences in dissolved DNA from aquatic environments , 1989, Microbial Ecology.

[110]  M. Maeda,et al.  Deoxyribonuclease activity in seawater and sediment , 1973 .

[111]  A. Dell'Anno,et al.  Degradation and Turnover of Extracellular DNA in Marine Sediments: Ecological and Methodological Considerations , 2004, Applied and Environmental Microbiology.

[112]  E. D. Earle,et al.  Nuclear DNA content of some important plant species , 2007, Plant Molecular Biology Reporter.

[113]  Z. Kawabata,et al.  Estimation of the fate of dissolved DNA in thermally stratified lake water from the stability of exogenous plasmid DNA , 2001 .

[114]  Leshchinskaia Ib,et al.  Nucleic acids utilized as the main source of bacterial nutrition , 1976 .

[115]  W. Klingmüller,et al.  DNA recovery and direct detection of Tn5 sequences from soil , 1991, Letters in applied microbiology.

[116]  Cécile Fairhead,et al.  Mitochondrial DNA repairs double-strand breaks in yeast chromosomes , 1999, Nature.

[117]  H. P. Zassenhaus,et al.  Sequence and expression of NUC1, the gene encoding the mitochondrial nuclease in Saccharomyces cerevisiae. , 1988, Nucleic acids research.

[118]  Jeffrey P Townsend,et al.  Monitoring and modeling horizontal gene transfer , 2004, Nature Biotechnology.

[119]  W Wackernagel,et al.  A conditional suicide system in Escherichia coli based on the intracellular degradation of DNA , 1994, Applied and environmental microbiology.

[120]  E. Rangarajan,et al.  Sugar non-specific endonucleases. , 2001, FEMS microbiology reviews.

[121]  C. Jeffries,et al.  ISOLATION AND PROPERTIES OF AN EXOCELLULAR NUCLEASE OF SERRATIA MARCESCENS , 1963, Journal of bacteriology.

[122]  R. Burns Enzyme activity in soil: Location and a possible role in microbial ecology , 1982 .

[123]  R. Palmen,et al.  Uptake and processing of DNA by Acinetobacter calcoaceticus--a review. , 1997, Gene.

[124]  K. Nielsen,et al.  Natural transformation and availability of transforming DNA to Acinetobacter calcoaceticus in soil microcosms , 1997, Applied and environmental microbiology.

[125]  R. Palmen,et al.  Acinetobacter calcoaceticus liberates chromosomal DNA during induction of competence by cell lysis , 2004, Current Microbiology.

[126]  Philipp Weller,et al.  The effect of processing parameters on DNA degradation in food , 2003 .

[127]  T. Vogel,et al.  Extraction of DNA from soil , 2003 .

[128]  M. G. Lorenz,et al.  Interaction of marine sediment with DNA and DNA availability to nucleases , 1981 .

[129]  S. Møller,et al.  Using inactivated microbial biomass as fertilizer: the fate of antibiotic resistance genes in the environment. , 2001, Research in microbiology.

[130]  A. Séguin,et al.  Assessing the persistence of DNA in decomposing leaves of genetically modified poplar trees , 2002 .

[131]  R. Daniel The metagenomics of soil , 2005, Nature Reviews Microbiology.

[132]  P. Normand,et al.  Kinetics of the persistence of chromosomal DNA from genetically engineered Escherichia coli introduced into soil , 1993, Applied and environmental microbiology.

[133]  N. Taga,et al.  Occurrence and distribution of deoxyribonucleic acid-hydrolyzing bacteria in sea water , 1974 .

[134]  G. Sayler,et al.  The extraction and purification of microbial DNA from sediments , 1987 .

[135]  E. Smit,et al.  Analysis of Fungal Diversity in the Wheat Rhizosphere by Sequencing of Cloned PCR-Amplified Genes Encoding 18S rRNA and Temperature Gradient Gel Electrophoresis , 1999, Applied and Environmental Microbiology.

[136]  T. Vogel,et al.  Degradation and Transformability of DNA from Transgenic Leaves , 2003, Applied and Environmental Microbiology.

[137]  J. Oades,et al.  The retention of organic matter in soils , 1988 .

[138]  G. Stotzky,et al.  Formation of Clay‐Protein Complexes , 1971 .

[139]  B. Spratt,et al.  Recombination and the population structures of bacterial pathogens. , 2001, Annual review of microbiology.

[140]  M. G. Lorenz,et al.  Mechanism of Retarded DNA Degradation and Prokaryotic Origin of DNases in Nonsterile Soils , 1997 .

[141]  P. Grace,et al.  The potential use of soil enzymes as indicators of productivity, sustainability and pollution. , 1994 .

[142]  F. Gagné,et al.  Occurrence and persistence of Bacillus thuringiensis (Bt) and transgenic Bt corn cry1Ab gene from an aquatic environment. , 2007, Ecotoxicology and environmental safety.

[143]  G. Stotzky,et al.  Gene transfer among bacteria in natural environments. , 1997, Advances in applied microbiology.

[144]  X. Nesme,et al.  Plant Genome Complexity May Be a Factor Limiting In Situ the Transfer of Transgenic Plant Genes to the PhytopathogenRalstonia solanacearum , 2000, Applied and Environmental Microbiology.

[145]  R. Seidler,et al.  Quantification of transgenic plant marker gene persistence in the field , 1997 .

[146]  M. G. Lorenz,et al.  Adsorption of DNA to sand and variable degradation rates of adsorbed DNA , 1987, Applied and environmental microbiology.

[147]  D. Deere,et al.  Survival of cells and DNA of Aeromonas salmonicida released into aquatic microcosms. , 1996, The Journal of applied bacteriology.

[148]  Lee,et al.  Transformation is a Mechanism of Gene Transfer in Soil , 1990 .

[149]  K. Nielsen,et al.  Stabilization of Extracellular DNA and Proteins by Transient Binding to Various Soil Components , 2006 .

[150]  A. Friedlander DNA release as a direct measure of microbial killing by phagocytes , 1978, Infection and immunity.

[151]  E. Kandeler,et al.  Enzyme Activities and Microbiological and Biochemical Processes in Soil , 2002 .

[152]  S. Ben‐Sasson,et al.  Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation , 1992, The Journal of cell biology.

[153]  C. Istock,et al.  Gene exchange and natural selection cause Bacillus subtilis to evolve in soil culture. , 1979, Science.

[154]  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 , 1991 .

[155]  K. Nielsen,et al.  Induced Natural Transformation of Acinetobacter calcoaceticus in Soil Microcosms , 1997, Applied and environmental microbiology.

[156]  U. Strych,et al.  Serratia marcescens and its extracellular nuclease. , 1998, FEMS microbiology letters.

[157]  M. Caprais,et al.  Salmonella DNA persistence in natural seawaters using PCR analysis , 1997, Journal of applied microbiology.

[158]  J. Paul,et al.  Dynamics of extracellular DNA in the marine environment , 1987, Applied and environmental microbiology.

[159]  J. V. van Elsas,et al.  Analysis of the dynamics of fungal communities in soil via fungal-specific PCR of soil DNA followed by denaturing gradient gel electrophoresis. , 2000, Journal of microbiological methods.