Skip to main content
SpringerLink
Log in

Gene Transfer Agents and Defective Bacteriophages as Sources of Extracellular Prokaryotic DNA

  • Chapter
  • First Online:
Extracellular Nucleic Acids

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

Abstract

A large amount of extracellular DNA on the planet exists in the form of viruses and virus-like particles. Globally, these particles contain a large amount of DNA that appears to have originated from cellular organism genomes, as opposed to being truly viral. Although the exact frequencies with which packaging of cellular DNA happens and the full range of reasons for why this happens are not known, virus-like elements that package host DNA are known. These include defective phages and gene transfer agents. The potential that these elements have to contribute to the pool of extracellular prokaryotic nucleic acids is discussed in this chapter.

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

Access this chapter

Log in via an institution
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

Institutional subscriptions

References

  • Anderson B, Goldsmith C, Johnson A, Padmalayam I, Baumstark B (1994) Bacteriophage-like particle of Rochalimaea henselae. Mol Microbiol 13:67–73

    Article  PubMed  CAS  Google Scholar 

  • Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, Chan AM, Haynes M, Kelley S, Liu H, Mahaffy JM, Mueller JE, Nulton J, Olson R, Parsons R, Rayhawk S, Suttle CA, Rohwer F (2006) The marine viromes of four oceanic regions. PLoS Biol 4:e368

    Article  PubMed  Google Scholar 

  • Barbian KD, Minnick MF (2000) A bacteriophage-like particle from Bartonella bacilliformis. Microbiology 146:599–609

    PubMed  CAS  Google Scholar 

  • Bertani G (1999) Transduction-like gene transfer in the methanogen Methanococcus voltae. J Bacteriol 181:2992–3002

    PubMed  CAS  Google Scholar 

  • Biers EJ, Wang K, Pennington C, Belas R, Chen F, Moran MA (2008) Occurrence and expression of gene transfer agent genes in marine bacterioplankton. Appl Environ Microbiol 74:2933–2939

    Article  PubMed  CAS  Google Scholar 

  • Bowers TJ, Sweger D, Jue D, Anderson B (1998) Isolation, sequencing and expression of the gene encoding a major protein from the backteriophage associated with Bartonella henselae. Gene 206:49–52

    Article  PubMed  CAS  Google Scholar 

  • Brinkhoff T, Giebel H-A, Simon M (2008) Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189:531–539

    Article  PubMed  CAS  Google Scholar 

  • Brussaard CPD, Marie D, Bratbak G (2000) Flow cytometric detection of viruses. J Virol Methods 85:175–182

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Buchan A, Gonzalez JM, Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71:5665–5677

    Article  PubMed  CAS  Google Scholar 

  • Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann M-L, Brussow H (2003a) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6:417–424

    Article  PubMed  CAS  Google Scholar 

  • Canchaya C, Proux C, Fournous G, Bruttin A, Brussow H (2003b) Prophage genomics. Microbiol Mol Biol Rev 67:238–276

    Article  PubMed  CAS  Google Scholar 

  • Casjens S (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49:277–300

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Hatfull G, Hendrix R (1992) Evolution of dsDNA tailed-bacteriophage genomes. Semin Virol 3:383–397

    CAS  Google Scholar 

  • Casjens S, Palmer N, van Vugt R, Huang WM, Stevenson B, Rosa P, Lathigra R, Sutton G, Peterson J, Dodson RJ, Haft D, Hickey E, Gwinn M, White O, Fraser CM (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35:490–516

    Article  PubMed  CAS  Google Scholar 

  • Cheetham BF, Katz ME (1995) A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol Microbiol 18:201–208

    Article  PubMed  CAS  Google Scholar 

  • Culley AI, Lang AS, Suttle CA (2006) Metagenomic analysis of coastal RNA virus communities. Science 312:1795–1798

    Article  PubMed  CAS  Google Scholar 

  • Danovaro R, Corinaldesi C, Filippini M, Fischer UR, Gessner MO, Jacquet S, Magagnini M, Velimirov B (2008) Viriobenthos in freshwater and marine sediments: a review. Freshwater Biol 53:1186–1213

    Article  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 

  • Djikeng A, Kuzmickas R, Anderson NG, Spiro DJ (2009) Metagenomic analysis of RNA viruses in a fresh water lake. PLoS One 4:e7264

    Article  PubMed  Google Scholar 

  • Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhawk S, Knight R, Rohwer F, Jackson RB (2007) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microbiol 73:7059–7066

    Article  PubMed  CAS  Google Scholar 

  • Garro AJ, Marmur J (1970) Defective bacteriophages. J Cell Physiol 76:253–264

    Article  PubMed  CAS  Google Scholar 

  • Genthner FJ, Wall JD (1984) Isolation of a recombination-deficient mutant of Rhodopseudomonas capsulata. J Bacteriol 160:971–975

    PubMed  CAS  Google Scholar 

  • Humphrey SB, Stanton TB, Jensen NS, Zuerner RL (1997) Purification and characterization of VSH-1, a generalized transducing bacteriophage of Serpulina hyodysenteriae. J Bacteriol 179:323–329

    PubMed  CAS  Google Scholar 

  • Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64:2780–2787

    PubMed  CAS  Google Scholar 

  • Lang AS, Beatty JT (2000) Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus. Proc Natl Acad Sci U S A 97:859–864

    Article  PubMed  CAS  Google Scholar 

  • Lang AS, Beatty JT (2001) The gene transfer agent of Rhodobacter capsulatus and “constitutive transduction” in prokaryotes. Arch Microbiol 175:241–249

    Article  PubMed  CAS  Google Scholar 

  • Lang AS, Beatty JT (2002) A bacterial signal transduction system controls genetic exchange and motility. J Bacteriol 184:913–918

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lang AS, Taylor TA, Beatty JT (2002) Evolutionary implications of phylogenetic analyses of the gene transfer agent (GTA) of Rhodobacter capsulatus. J Mol Evol 55:534–543

    Article  PubMed  CAS  Google Scholar 

  • Lilburn TG, Haith CE, Prince RC, Beatty JT (1992) Pleiotropic effects of pufX gene deletion on the structure and function of the photosynthetic apparatus of Rhodobacter capsulatus. Biochim Biophys Acta Bio 1100:160–170

    Article  CAS  Google Scholar 

  • Madigan MT, Jung DO (2009) An overview of Purple Bacteria: systematics, physiology, and habitats. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The Purple Phototrophic Bacteria. Springer, New York, pp 1–15

    Chapter  Google Scholar 

  • Marrs BL (1974) Genetic recombination in Rhodopseudomonas capsulata. Proc Natl Acad Sci USA 71:971–973

    Article  PubMed  CAS  Google Scholar 

  • Marrs BL (1978) Mutations and genetic manipulations as probes of bacterial photosynthesis. Curr Top Bioenerget 8:261–294

    CAS  Google Scholar 

  • Matson EG, Thompson MG, Humphrey SB, Zuerner RL, Stanton TB (2005) Identification of genes of VSH-1, a prophage-like gene transfer agent of Brachyspira hyodysenteriae. J Bacteriol 187:5885–5892

    Article  PubMed  CAS  Google Scholar 

  • Matson EG, Zuerner RL, Stanton TB (2007) Induction and transcription of VSH-1, a prophage-like gene transfer agent of Brachyspira hyodysenteriae. Anaerobe 13:89–97

    Article  PubMed  CAS  Google Scholar 

  • Motro Y, La T, Bellgard MI, Dunn DS, Phillips ND, Hampson DJ (2009) Identification of genes associated with prophage-like gene transfer agents in the pathogenic intestinal spirochaetes Brachyspira hyodysenteriae, Brachyspira pilosicoli and Brachyspira intermedia. Vet Microbiol 134:340–345

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  PubMed  CAS  Google Scholar 

  • Okamoto K, Mudd JA, Mangan J, Huang WM, Subbaiah TV, Marmur J (1968) Properties of the defective phage of Bacillus subtilis. J Mol Biol 34:413–428

    Article  PubMed  CAS  Google Scholar 

  • Rapp BJ, Wall JD (1987) Genetic transfer in Desulfovibrio desulfuricans. Proc Natl Acad Sci USA 84:9128–9130

    Article  PubMed  CAS  Google Scholar 

  • Schaefer AL, Taylor TA, Beatty JT, Greenberg EP (2002) Long-chain acyl-homoserine lactone quorum-sensing regulation of Rhodobacter capsulatus gene transfer agent production. J Bacteriol 184:6515–6521

    Article  PubMed  CAS  Google Scholar 

  • Schoenfeld T, Patterson M, Richardson PM, Wommack KE, Young M, Mead D (2008) Assembly of viral metagenomes from Yellowstone hot springs. Appl Environ Microbiol 74:4164–4174

    Article  PubMed  CAS  Google Scholar 

  • Scolnik PA, Haselkorn R (1984) Activation of extra copies of genes coding for nitrogenase in Rhodopseudomonas capsulata. Nature 307:289–292

    Article  PubMed  CAS  Google Scholar 

  • Scolnik PA, Marrs BL (1987) Genetic research with photosynthetic bacteria. Ann Rev Microbiol 41:703–726

    Article  CAS  Google Scholar 

  • Seaman E, Tarmy E, Marmur J (1964) Inducible phages of Bacillus subtilis. Biochemistry 3:607–613

    Article  PubMed  CAS  Google Scholar 

  • Solioz M, Marrs B (1977) The gene transfer agent of Rhodopseudomonas capsulata: purification and characterization of its nucleic acid. Arch Biochem Biophys 181:300–307

    Article  PubMed  CAS  Google Scholar 

  • Solioz M, Yen H-C, Marrs B (1975) Release and uptake of gene transfer agent by Rhodopseudomonas capsulata. J Bacteriol 123:651–657

    PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Stanton TB, Thompson MG, Humphrey SB, Zuerner RL (2003) Detection of bacteriophage VSH-1 svp38 gene in Brachyspira spirochetes. FEMS Microbiol Lett 224:225–229

    Article  PubMed  CAS  Google Scholar 

  • Stanton TB, Humphrey SB, Bayles DO, Zuerner RL (2009) Identification of a divided genome for VSH-1, the prophage-like gene transfer agent of Brachyspira hyodysenteriae. J Bacteriol 191:1719–1721

    Article  PubMed  CAS  Google Scholar 

  • Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    Article  PubMed  CAS  Google Scholar 

  • Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  PubMed  CAS  Google Scholar 

  • Tsutsumi Y, Hirokawa H, Shishido K (1990) A new defective phage containing a randomly selected 8 kilobase-pairs fragment of host chromosomal DNA inducible in a strain of Bacillus natto. FEMS Microbiol Lett 72:41–46

    Article  CAS  Google Scholar 

  • Vos M (2009) Why do bacteria engage in homologous recombination? Trends Microbiol 17:226–232

    Article  PubMed  CAS  Google Scholar 

  • Wagner-Dobler I, Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60:255–280

    Article  PubMed  Google Scholar 

  • Wall JD, Braddock K (1984) Mapping of Rhodopseudomonas capsulata nif genes. J Bacteriol 158:404–410

    PubMed  CAS  Google Scholar 

  • Wall JD, Weaver PF, Gest H (1975a) Gene transfer agents, bacteriophages, and bacteriocins of Rhodopseudomonas capsulata. Arch Microbiol 105:217–224

    Article  PubMed  CAS  Google Scholar 

  • Wall JD, Weaver PF, Gest H (1975b) Genetic transfer of nitrogenase-hydrogenase activity in Rhodopseudomonas capsulata. Nature 258:630–631

    Article  PubMed  CAS  Google Scholar 

  • Wen K, Ortmann AC, Suttle CA (2004) Accurate estimation of viral abundance by epifluorescence microscopy. Appl Environ Microbiol 70:3862–3867

    Article  PubMed  CAS  Google Scholar 

  • Williamson KE, Radosevich M, Wommack KE (2005) Abundance and diversity of viruses in six Delaware soils. Appl Environ Microbiol 71:3119–3125

    Article  PubMed  CAS  Google Scholar 

  • Wood HE, Dawson MT, Devine KM, McConnell DJ (1990) Characterization of PBSX, a defective prophage of Bacillus subtilis. J Bacteriol 172:2667–2674

    PubMed  CAS  Google Scholar 

  • Yen H-C, Marrs B (1976) Map of genes for carotenoid and bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata. J Bacteriol 126:619–629

    PubMed  CAS  Google Scholar 

  • Yen H-C, Hu NT, Marrs BL (1979) Characterization of the gene transfer agent made by an overproducer mutant of Rhodopseudomonas capsulata. J Mol Biol 131:157–168

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Barry Marrs, Judy Wall, and Thad Stanton for permission to use EM images of RcGTA, Dd1, and VSH-1, respectively. We are grateful for research support from the Canadian Natural Sciences and Engineering Research Council (A.S.L.), and the Killam Trust and Canadian Institutes of Health Research (J.T.B).

Author information

Authors and Affiliations

  1. Department of Biology, Memorial University of Newfoundland, St. John’s, NL, Canada, A1B 3X9

    Andrew S. Lang

  2. Department of Microbiology and Immunology, University of British Columbia, Vancouver, BC, Canada, V6T 1Z3

    J. Thomas Beatty

Authors
  1. Andrew S. Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Thomas Beatty
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew S. Lang .

Editor information

Editors and Affiliations

  1. , Dept. of Environmental and Life Sciences, Toyohashi University of Technology, Toyohashi-city, 441-8580, Japan

    Yo Kikuchi

  2. Fundamental Medicine, Institute of Chemical Biology and, Lavrentjeva Prospect 8, Novosibirsk, 630090, Russian Federation

    Elena Y. Rykova

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Lang, A.S., Beatty, J.T. (2010). Gene Transfer Agents and Defective Bacteriophages as Sources of Extracellular Prokaryotic DNA. 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_2

Download citation

Publish with us

Policies and ethics

Search

Navigation