Skip to main content
Log in

Importance of Viral Lysis and Dissolved DNA for Bacterioplankton Activity in a P-Limited Estuary, Northern Baltic Sea

  • Original Article
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Through lysis of bacterioplankton cells, viruses mediate an important, but poorly understood, pathway of carbon and nutrients from the particulate to the dissolved form. Via this activity, nutrient-rich cell lysates may become available to noninfected cells and support significant growth. However, the nutritional value of lysates for noninfected bacteria presumably depends on the prevailing nutrient limitation. In the present study, we examined dynamics of dissolved DNA (D-DNA) and viruses along a transect in the phosphorus (P)-limited Öre Estuary, northern Baltic Sea. We found that viruses were an important mortality factor for bacterioplankton and that their activity mediated a significant recycling of carbon and especially of P. Uptake of dissolved DNA accounted for up to 70% of the bacterioplankton P demand, and about a quarter of the D-DNA pool was supplied through viral lysis of bacterial cells. Generally, the importance of viral lysates and uptake of D-DNA was highest at the estuarine and offshore stations and was positively correlated with P limitation measured as alkaline phosphatase activity. Our results highlight the importance of viral activity for the internal recycling of principal nutrients and pinpoints D-DNA as a particularly relevant compound in microbial P dynamics.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Alonso MC, Rodriguez J, Borrego JJ (1999) Role of ciliates, flagellates and bacteriophages on the mortality of marine bacteria and on dissolved-DNA concentration in laboratory experimental systems. J Exp Mar Biol Ecol 244:239–252

    Article  Google Scholar 

  2. Ammerman JW, Azam F (1985) Bacterial 5′-nucleotidase in aquatic ecosystems: a novel mechanism of phosphorus regeneration. Science 227:1338–1340

    Article  PubMed  CAS  Google Scholar 

  3. Blackburn N, Zweifel UL, Hagström Å (1996) Cycling of marine dissolved organic matter. II. A model analysis. Aquat Microb Ecol 11:79–90

    Article  Google Scholar 

  4. Bongiorni L, Magagnini M, Armeni M, Noble R, Danovaro R (2005) Viral production, decay rates, and life strategies along a trophic gradient in the North Adriatic Sea. Appl Environ Microbiol 71:6644–6650

    Article  PubMed  CAS  Google Scholar 

  5. Brum JR (2005) Concentration, production and turnover of viruses and dissolved DNA pools at Stn ALOHA, North Pacific Subtropical Gyre. Aquat Microb Ecol 41:103–113

    Article  Google Scholar 

  6. Brum JR, Steward GF, Karl DM (2004) A novel method for the measurement of dissolved deoxyribonucleic acid in seawater. Limnol Oceanogr Methods 2:248–255

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  8. DeFlauen MF, Paul JH, Jeffrey WH (1987) Distribution and molecular weight of dissolved DNA in subtropical estuarine and oceanic environments. Mar Ecol Prog Ser 38:65–73

    Article  Google Scholar 

  9. Filippini M, Middelboe M (2007) Viral abundance and genome size distribution in the sediment and water column of marine and freshwater ecosystems. FEMS Microbiol Ecol 60:397–410

    Article  PubMed  CAS  Google Scholar 

  10. Fuhrman JA (1992) Bacterioplankton roles in cycling of organic matter: the microbial food web. In: Falkowski PG, Woodhead AD (eds) Primary productivity and biogeochemical cycles in the sea. Plenum, New York, pp 361–383

    Google Scholar 

  11. Fuhrman JA, Azam F (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar Biol 66:109–120

    Article  Google Scholar 

  12. Fuhrman JA, Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40:1236–1242

    Google Scholar 

  13. Hagström Å, Larsson U (1984) Diel and seasonal variation in growth rates of pelagic bacteria. In: Hobbie JE, Williams PJLB (eds) Heterotrophic activity in the sea. Plenum, New York, pp 249–262

    Google Scholar 

  14. Hewson I, O’Neil JM, Fuhrman JA, Dennison WC (2001) Virus-like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries. Limnol Oceanogr 46:1734–1746

    Google Scholar 

  15. Jeffrey WH, Von Haven R, Hoch MP, Coffin RB (1996) Bacterioplankton RNA, DNA protein content and relationships to rates of thymidine and leucine incorporation. Aquat Microb Ecol 10:87–95

    Article  Google Scholar 

  16. Jiang SC, Paul JH (1995) Viral contribution to dissolved DNA in the marine environment as determined by differential centrifugation and kingdom probing. Appl Environ Microbiol 61:317–325

    PubMed  CAS  Google Scholar 

  17. Jørgensen NOG, Jacobsen CS (1996) Bacterial uptake and utilization of dissolved DNA. Aquat Microb Ecol 11:263–270

    Article  Google Scholar 

  18. Marie D, Brussaard CPD, Thyrhaug R, Bratbak G, Vaulot D (1999) Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl Environ Microbiol 65:45–52

    PubMed  CAS  Google Scholar 

  19. Middelboe M, Jørgensen NOG (2006) Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds. J Mar Biol Ass U K 86:605–612

    Article  CAS  Google Scholar 

  20. Middelboe M, Jørgensen NOG, Kroer N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62:1991–1997

    PubMed  Google Scholar 

  21. Middelboe M, Lyck PG (2002) Regeneration of dissolved organic matter by viral lysis in marine microbial communities. Aquat Microb Ecol 27:187–194

    Article  Google Scholar 

  22. Middelboe M, Riemann L, Steward GF, Hansen V, Nybroe O (2003) Virus-induced transfer of organic matter between marine bacteria in a model community. Aquat Microb Ecol 33:1–10

    Article  Google Scholar 

  23. Minear RA (1972) Characterization of naturally occurring dissolved organophosphorus compounds. Env Sci Tech 6:431–437

    Article  CAS  Google Scholar 

  24. Nausch M (1998) Alkaline phosphatase activities and the relationship to inorganic phosphate in the Pomeranian Bight (southern Baltic Sea). Aquat Microb Ecol 16:87–94

    Article  Google Scholar 

  25. Noble RT, Fuhrman JA (1998) Use of SYBR green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14:113–118

    Article  Google Scholar 

  26. Noble RT, Fuhrman JA (1999) Breakdown and microbial uptake of marine viruses and other lysis products. Aquat Microb Ecol 20:1–11

    Article  Google Scholar 

  27. Parada V, Herndl GJ, Weinbauer MG (2006) Viral burst size of heterotrophic prokaryotes in aquatic systems. J Mar Biol Ass U K 86:613–621

    Article  Google Scholar 

  28. Paul JH, Jeffrey WH, DeFlauen MF (1986) Dynamics of extracellular DNA in the marine environment. Appl Environ Microbiol 53:170–179

    Google Scholar 

  29. Paul JH, DeFlaun MF, Jeffrey WH, David AW (1988) Seasonal and diel variability in dissolved DNA and in microbial biomass and activity in a subtropical estuary. Appl Environ Microbiol 54:718–727

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  31. Riemann L, Middelboe M (2002) Stability of bacterial and viral community compositions in Danish coastal waters as depicted by DNA fingerprinting techniques. Aquat Microb Ecol 27:219–232

    Article  Google Scholar 

  32. Riemann L, Leitet C, Pommier T, Simu K, Holmfeldt K, Larsson U, Hagström Å (2008) The native bacterioplankton community in the central Baltic sea is influenced by freshwater bacterial species. Appl Environ Microbiol 74:503–515

    Article  PubMed  CAS  Google Scholar 

  33. Sandberg J, Andersson A, Johansson S, Wikner J (2004) Pelagic food web structure and carbon budget in the northern Baltic Sea: potential importance of terrigenous carbon. Mar Ecol Prog Ser 268:13–29

    Article  Google Scholar 

  34. Siuda W, Chróst RJ, Gude H (1998) Distribution and origin of dissolved DNA in lakes of different trophic states. Aquat Microb Ecol 15:89–96

    Article  Google Scholar 

  35. Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114

    Google Scholar 

  36. Steward GF (2000) Fingerprinting viral assemblages by pulsed field gel electrophoresis (PFGE). In: Paul JH (ed) Marine microbiology, methods in microbiology. Academic, New York, pp 85–103

    Google Scholar 

  37. Steward GF, Montiel JL, Azam F (2000) Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol Oceanogr 45:1697–1706

    Google Scholar 

  38. Tezuka Y (1990) Bacterial regeneration of ammonium and phosphate as affected by the carbon:nitrogen:phosphorus ratio of organic substrates. Microb Ecol 19:227–238

    Article  CAS  Google Scholar 

  39. Titelman J, Riemann L, Holmfeldt K, Nilsen T (2008) Copepod feeding stimulates bacterioplankton activities in a low phosphorus system. Aquat Biol 2:131–141

    Article  Google Scholar 

  40. Troussellier M, Courties C, Lebaron P, Servais P (1999) Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids. FEMS Microbiol Ecol 29:319–330

    Article  CAS  Google Scholar 

  41. 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 

  42. Weinbauer MG, Fuks D, Peduzzi P (1993) Distribution of viruses and dissolved DNA along a coastal trophic gradient in the northern Adriatic sea. Appl Environ Microbiol 59:4074–4082

    PubMed  CAS  Google Scholar 

  43. Weinbauer MG, Fuks D, Puskaric S, Peduzzi P (1995) Diel, seasonal, and depth-related variability of viruses and dissolved DNA in the Northern Adriatic Sea. Microb Ecol 30:25–41

    Article  Google Scholar 

  44. Weinbauer MG, Brettar I, Höfle MG (2003) Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48:1457–1465

    Google Scholar 

  45. Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea. BioSci 49:781–788

    Article  Google Scholar 

  46. Wilhelm SW, Bridgen SM, Suttle CA (2002) A dilution technique for the direct measurement of viral production: a comparison in stratified and tidally mixed coastal waters. Microb Ecol 43:168–173

    Article  PubMed  CAS  Google Scholar 

  47. Winget DM, Williamson KE, Helton RR, Wommack KE (2005) Tangential flow diafiltration: an improved technique for estimation of virioplankton production. Aquat Microb Ecol 41:221–232

    Article  Google Scholar 

  48. Winter C, Herndl GJ, Weinbauer MG (2004) Diel cycles in viral infection of bacterioplankton in the North Sea. Aquat Microb Ecol 35:207–216

    Article  Google Scholar 

  49. Zweifel UL, Norrman B, Hagström Å (1993) Consumption of dissolved organic matter by marine bacteria and demand for inorganic nutrients. Mar Ecol Prog Ser 101:23–32

    Article  CAS  Google Scholar 

  50. Zweifel UL, Wikner J, Hagström Å, Lundberg E, Norrman B (1995) Dynamics of dissolved organic carbon in a coastal ecosystem. Limnol Oceanogr 40:299–305

    CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Stangenberg and the rest of the staff for helping us find our way at the Umeå Marine Sciences Center. We thank J. Wester and M. Molin for help in the field, J. Wikner for providing the thymidine conversion factor, and B. Olsen, University of Kalmar, for use of PFGE equipment. This study was supported by a guest research grant from Umeå Marine Sciences Center to JT and LR and a grant from FORMAS (2006-1054) to JT.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lasse Riemann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Riemann, L., Holmfeldt, K. & Titelman, J. Importance of Viral Lysis and Dissolved DNA for Bacterioplankton Activity in a P-Limited Estuary, Northern Baltic Sea. Microb Ecol 57, 286–294 (2009). https://doi.org/10.1007/s00248-008-9429-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-008-9429-0

Keywords

Navigation