Skip to main content

Roles of Extracellular DNA in Bacterial Ecosystem

  • Chapter
  • First Online:

Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 25))

Abstract

Extracellular DNA in the natural environment is a source of nutrients and gene pools for bacteria. In sediments and biofilms, gene transfer must occur among bacteria via extracellular DNA because the concentrations of both exogenous DNA and cells are high. Some bacteria actively release naked DNA or the membrane vesicle containing the DNA into the environment. Some bacteria also produce extracellular DNA by suicide and fratricide. Released DNA is used for DNA repair, transformation, and generation of genetic diversity. DNA is required for the initiation of biofilm formation and stabilization of biofilms. In biofilms, gene exchange and mutation must occur to generate diversity.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Ambur OH, Stephan A, Tønjum T (2007) New functional identity for the DNA uptake sequence. J Bacteriol 189:2077–2085

    Article  PubMed  CAS  Google Scholar 

  • Assalkhou A, Balasingham S, Collins RF, Frye SA, Davidsen T, Benam AV, Bjørås M, Derrick JP, Tønjum T (2007) The outer membrane secretin PilQ from Neisseria meningitidis binds DNA. Microbiology 153:1593–1603

    Article  PubMed  CAS  Google Scholar 

  • Bakkali M, Chen T-Y, Lee HC, Redfield RJ (2004) Evolutionary stability of DNA uptake signal sequences in the Pasteurellaceae. Proc Natl Acad Sci U S A 101:4513–4518

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen I, Christie PJ, Dubnau D (2005) The ins and outs of DNA transfer in bacteria. Science 310:1456–1460

    Article  PubMed  CAS  Google Scholar 

  • Corinaldesi C, Danovaro R, Dell’Anno A (2005) Simultaneous recovery of extracellular and intracellular DNA suitable for molecular studies from marine sediments. Appl Environ Microbiol 71:46–50

    Article  PubMed  CAS  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    Article  PubMed  CAS  Google Scholar 

  • Danner DB, Deich RA, Sisco KL, Smith HO (1980) An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene 11:311–318

    Article  PubMed  CAS  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 U S A 99:2094–2099

    Article  PubMed  Google Scholar 

  • DeFlaun MF, Paul JH, Davis D (1986) Simplified method for dissolved DNA determination in aquatic environments. Appl Environ Microbiol 52:654–659

    PubMed  CAS  Google Scholar 

  • DeFlaun MF, Paul JH, Wade HJ (1987) Distribution and molecular weight of dissolved DNA in subtropical estuarine and oceanic environments. Mar Ecol Prog Ser 38:65–73

    Article  CAS  Google Scholar 

  • Dell’Anno A, Corinaldesi C (2004) Degradation and turnover of extracellular DNA in marine sediments: ecological and methodological considerations. Appl Environ Microbiol 70:4384–4386

    Article  PubMed  Google Scholar 

  • Dell'Anno A, Danovaro R (2005) Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science 309:2179

    Article  PubMed  Google Scholar 

  • Dell'Anno A, Fabiano M, Mei ML, Danovaro R (1999) Pelagic-benthic coupling of nucleic acids in an abyssal location of the Northeastern Atlantic ocean. Appl Environ Microbiol 65:4451–4457

    PubMed  Google Scholar 

  • Driffield K, Miller K, Bostock JM, O'Neill AJ, Chopra I (2008) Increased mutability of Pseudomonas aeruginosa in biofilms. J Antimicrob Chemother 61:1053–1056

    Article  PubMed  CAS  Google Scholar 

  • Dubnau D (1999) DNA uptake in bacteria. Annu Rev Microbiol 53:217–244

    Article  PubMed  CAS  Google Scholar 

  • Finkel SE, Kolter R (2001) DNA as a nutrient: novel role for bacterial competence gene homologs. J Bacteriol 183:6288–6293

    Article  PubMed  CAS  Google Scholar 

  • Goodman SD, Scocca JJ (1988) Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc Natl Acad Sci U S A 85:6982–6986

    Article  PubMed  CAS  Google Scholar 

  • Graves JF, Biswas GD, Sparlingi PF (1982) Sequence-specific DNA uptake in transformation of Neisseria gonorrhoeae. J Bacteriol 152:1071–1077

    PubMed  CAS  Google Scholar 

  • Hamilton HL, Dillard PJ (2006) Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol 59:376–385

    Article  PubMed  CAS  Google Scholar 

  • Hamilton HL, Domínguez NM, Schwartz KJ, Hackett KT, Dillard PJ (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55:1704–1721

    Article  PubMed  CAS  Google Scholar 

  • Hendrickx L, Hausner M, Wuertz S (2003) Natural genetic transformation in monoculture Acinetobacter sp. strain BD413 biofilms. Appl Environ Microbiol 69:1721–1727

    Article  PubMed  CAS  Google Scholar 

  • Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74:470–476

    Article  PubMed  CAS  Google Scholar 

  • Karl DM, Bailiff MD (1989) The measurement and distribution of dissolved nucleic acids in aquatic environments. Limnol Oceanogr 34:543–558

    Article  CAS  Google Scholar 

  • Kenzaka T, Tamaki S, Yamaguchi KT, Nasu M (2005) Recognition of individual genes in diverse microorganisms by cycling primed in situ amplification. Appl Environ Microbiol 71:7236–7244

    Article  PubMed  CAS  Google Scholar 

  • Kolling GL, Matthews KR (1999) Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl Environ Microbiol 65:1843–1848

    PubMed  CAS  Google Scholar 

  • Lennon JT (2007) Diversity and metabolism of marine bacteria cultivated on dissolved DNA. Appl Environ Microbiol 73:2799–2805

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Clarke AJ, Beveridge TJ (1996) A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles. J Bacteriol 178:2479–2488

    PubMed  CAS  Google Scholar 

  • Liu H-H, Yang Y-R, Shen X-C, Zhang Z-L, Shen P, Xie Z-X (2008) Role of DNA in bacterial aggregation. Curr Microbiol 57:139–144

    Article  PubMed  Google Scholar 

  • Lorenz MG, Wackernagel W (1987) Adsorption of DNA to sand and variable degradation rates of adsorbed DNA. Appl Environ Microbiol 53:2948–2952

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Maruyama F, Kenzaka T, Yamaguchi N, Tani K, Nasu M (2003) Detection of bacteria carrying the stx2 gene by in situ loop-mediated isothermal amplification. Appl Environ Microbiol 69:5023–5028

    Article  PubMed  CAS  Google Scholar 

  • Maruyama F, Tani K, Kenzaka T, Yamaguchi N, Nasu M (2006) Quantitative determination of free-DNA uptake in river bacteria at the single-cell level by in situ rolling-circle amplification. Appl Environ Microbiol 72:6248–6256

    Article  PubMed  CAS  Google Scholar 

  • Matsui K, Ishii N, Kawabata Z (2003) Release of extracellular transformable plasmid DNA from Escherichia coli cocultivated with algae. Appl Environ Microbiol 69:2399–2404

    Article  PubMed  CAS  Google Scholar 

  • McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ (2006) Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 188:5385–5392

    Article  PubMed  CAS  Google Scholar 

  • Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathogens 4:e1000213

    Article  PubMed  Google Scholar 

  • Nakamura S, Higashiyama Y, Izumikawa K, Seki M, Kakeya H, Yamamoto Y, Yanagihara K, Miyazaki Y, Mizuta Y, Kohno S (2008) The roles of the quorum-sensing system in the release of extracellular DNA, lipopolysaccharide, and membrane vesicles from Pseudomonas aeruginosa. Jpn J Infect Dis 61:375–378

    PubMed  CAS  Google Scholar 

  • Niels O, Jorgensen G, Kroer N, Coffin RB (1994) Utilization of dissolved nitrogen by heterotrophic bacterioplankton: effect of substrate C/N Ratio. Appl Environ Microbiol 60:4124–4133

    Google Scholar 

  • Niemeye J, Gessler F (2002) Determination of free DNA in soils. J Plant Nutr Soil Sci 165:121–124

    Article  Google Scholar 

  • Ogram AV, Mathot ML, Harsh JB, BOYLE J, Pettigrew CA Jr (1994) Effects of DNA polymer length on its adsorption to soils. Appl Environ Microbiol 60:393–396

    PubMed  CAS  Google Scholar 

  • Palchevskiy V, Finkel SE (2006) Escherichia coli competence gene homologs are essential for competitive fitness and the use of DNA as a nutrient. J Bacteriol 188:3902–3910

    Article  PubMed  CAS  Google Scholar 

  • Paul JH, Jeffrey WH, DeFlaun MF (1987) Dynamics of extracellular DNA in the marine environment. Appl Environ Microbiol 53:170–179

    PubMed  CAS  Google Scholar 

  • Paul JH, Jeffrey WH, David AW, Deflaun MF, Cazares LH (1989) Turnover of extracellular DNA in eutrophic and oligotrophic freshwater environments of soutthwest Florida. Appl Environ Microbiol 55:1823–1828

    PubMed  CAS  Google Scholar 

  • Paul JH, Jiang SC, Rose JB (1991) Concentration of viruses and dissolved DNA from aquatic environments by vortex flow filtration. Appl Environ Microbiol 57:2197–2204

    PubMed  CAS  Google Scholar 

  • Petersen FC, Tao L, Scheie AA (2005) DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J Bacteriol 187:4392–4400

    Article  PubMed  CAS  Google Scholar 

  • Pinchuk GE, Ammons C, Culley DE, Li S-MW, McLean JS, Romine MF, Nealson KH, Fredrickson JK, Beliaev AS (2008) Utilization of DNA as a sole source of phosphorus, carbon, and Energy by Shewanella spp.: ecological and physiological implications for dissimilatory metal reduction. Appl Environ Microbiol 74:1198–1208

    Article  PubMed  CAS  Google Scholar 

  • Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083–2092

    Article  PubMed  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 J-M, Daffonchio D (2008) Strategy for in situ detection of natural transformation-based horizontal gene transfer events. Appl Environ Microbiol 74:1250–1254

    Article  PubMed  CAS  Google Scholar 

  • Romanowski G, Lorenz MG, Wackernagel W (1991) Adsorption of plasmid DNA to mineral surfaces and protection against DNase I. Appl Environ Microbiol 57:1057–1061

    PubMed  CAS  Google Scholar 

  • Scocca JJ, Poland RL, Zoon KC (1974) Specificity in deoxyribonucleic acid uptake by transformable Haemophilus influenza. J Bacteriol 118:369–373

    PubMed  CAS  Google Scholar 

  • Siuda W, Güde H (1996) Determination of dissolved deoxyribonucleic acid concentration in lake water. Aquat Microb Ecol 11:193–202

    Article  Google Scholar 

  • Steinberger RE, Holden PA (2004) Macromolecular composition of unsaturated Pseudomonas aeruginosa biofilms with time and carbon source. Biofims 1:37–47

    Article  Google Scholar 

  • Steinmoen H, Knutsen E, Håvarstein LS (2002) Iduction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. Proc Natl Acad Sci U S A 99:7681–7686

    Article  PubMed  CAS  Google Scholar 

  • Steinmoen H, Teigen A, Håvarstein LS (2003) Competence-induced cells of Streptococcus pneumoniae lyse competence-deficient cells of the same strain during cocultivation. J Bacteriol 185:7176–7183

    Article  PubMed  CAS  Google Scholar 

  • Stewart GJ, Sinigalliano CD (1990) Detection of horizontal gene transfer by natural transformation in native and introduced species of bacteria in marine and synthetic sediments. Appl Environ Microbiol 56:1818–1824

    PubMed  CAS  Google Scholar 

  • Tani K, Kurokawa K, Nasu M (1998) Development of a direct in situ PCR method for detection of specific bacteria in natural environments. Appl Environ Microbiol 64:1536–1540

    PubMed  CAS  Google Scholar 

  • Thomas VC, Thurlow LR, Boyle D, Hancock LE (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190:5690–5698

    Article  PubMed  CAS  Google Scholar 

  • Turk V, Rehnstam A-S, Lundberg E, Hagström Å (1992) Release of bacterial DNA by marine nanoflagellates, an intermediate step in phosphorus regeneration. Appl Environ Microbiol 58:3744–3750

    PubMed  CAS  Google Scholar 

  • Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JC (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wojciechowski MF, Hoelzer MA, Michod RE (1989) DNA repair and the evolution of transformation in Bacillus subtilis II. Role of inducible repair. Genetics 121(41):1–422

    Google Scholar 

  • Yang L, Skindersoe BKB, ME CAB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153:1318–1328

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masao Nasu .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Tani, K., Nasu, M. (2010). Roles of Extracellular DNA in Bacterial Ecosystem. In: Kikuchi, Y., Rykova, E. (eds) Extracellular Nucleic Acids. Nucleic Acids and Molecular Biology, vol 25. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12617-8_3

Download citation

Publish with us

Policies and ethics