Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Contributions of microbial biofilms to ecosystem processes in stream mesocosms

Abstract

In many aquatic ecosystems, most microbes live in matrix-enclosed biofilms1,2,3 and contribute substantially to energy flow and nutrient cycling. Little is known, however, about the coupling of structure and dynamics of these biofilms to ecosystem function2. Here we show that microbial biofilms changed the physical and chemical microhabitat and contributed to ecosystem processes in 30-m-long stream mesocosms. Biofilm growth increased hydrodynamic transient storage—streamwater detained in quiescent zones, which is a major physical template for ecological processes in streams4,5—by 300% and the retention of suspended particles by 120%. In addition, by enhancing the relative uptake of organic molecules of lower bioavailability, the interplay of biofilm microarchitecture and mass transfer changed their downstream linkage. As living zones of transient storage, biofilms bring hydrodynamic retention and biochemical processing into close spatial proximity and influence biogeochemical processes and patterns in streams. Thus, biofilms are highly efficient and successful ecological communities that may also contribute to the influence that headwater streams have on rivers, estuaries and even oceans6,7 through longitudinal linkages of local biogeochemical and hydrodynamic processes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Purchase on Springer Link

Instant access to full article PDF

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Effects of flow on biofilm structure and microarchitecture.
Figure 2
Figure 3: Temporal dynamics of the deposition velocity of suspended organic particles (a) and of the ratio between the mass transfer coefficients for arabinose and glucose (b).

Similar content being viewed by others

References

  1. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R. & Lappin-Scott, H. M. Microbial biofilms. Annu. Rev. Microbiol. 49, 711–745 (1995)

    Article  CAS  Google Scholar 

  2. Palmer, R. J. & White, D. C. Developmental biology of biofilms: implications for treatment and control. Trends Microbiol. 5, 435–440 (1997)

    Article  Google Scholar 

  3. Sutherland, I. W. The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol. 9, 222–227 (2001)

    Article  CAS  Google Scholar 

  4. Jones, J. B. & Mulholland, P. J. Streams and Ground Waters (Academic, San Diego, London, 2000)

    Google Scholar 

  5. Peterson, B. J. et al. Control of nitrogen export from watersheds by headwater streams. Science 292, 86–90 (2001)

    Article  ADS  CAS  Google Scholar 

  6. Alexander, R. B., Smith, R. A. & Schwarz, G. E. Effect of stream channel size on the delivery of nitrogen to the Gulf of Mexico. Nature 403, 758–761 (2000)

    Article  ADS  CAS  Google Scholar 

  7. Gomi, T., Sidle, R. C. & Richardson, J. S. Understanding processes and downstream linkages of headwater systems. Bioscience 52, 905–916 (2002)

    Article  Google Scholar 

  8. Packman, A. I., Brooks, N. H. & Morgan, J. J. A physicochemical model for colloid exchange between a stream and a sand bed with bed forms. Wat. Resour. Res. 36, 2351–2361 (2000)

    Article  ADS  CAS  Google Scholar 

  9. Mulholland, P. J., Steinman, A. D., Marzholf, E. R., Hart, D. R. & DeAngelis, D. L. Effect of periphyton biomass on hydraulic characteristics and nutrient cycling in streams. Oecologia 8, 40–47 (1994)

    Article  ADS  Google Scholar 

  10. Kim, B. K. & Jackman, A. P. Modeling transient storage and nitrate uptake kinetics in a flume containing a natural periphyton community. Wat. Resour. Res. 26, 505–515 (1990)

    Article  ADS  CAS  Google Scholar 

  11. Kugaprasatham, S., Nagaka, H. & Ohgaki, S. Effect of turbulence on nitrifying biofilms at non-limiting substrate conditions. Water Res. 26, 1629–1638 (1992)

    Article  CAS  Google Scholar 

  12. Minshall, G. W., Thomas, S. A., Newbold, J. D., Monaghan, M. T. & Cushing, C. E. Physical factors influencing fine organic particle transport and deposition in streams. J. N. Am. Benthol. Soc. 19, 1–16 (2000)

    Article  Google Scholar 

  13. Thomas, S. A. et al. The influence of particle size on seston deposition in streams. Limnol. Oceanogr. 46, 1415–1424 (2001)

    Article  ADS  Google Scholar 

  14. Drury, W. J., Characklis, W. G. & Stewart, P. S. Interactions of 1 µm latex particles with Pseudomonas aeruginosa biofilms. Water Res. 27, 1119–1126 (1993)

    Article  CAS  Google Scholar 

  15. Grady, C. P. L. Jr, Daigger, G. T. & Lim, H. C. Biological Wastewater Treatment 2nd edn (Marcel Dekker, New York, 1999)

    Google Scholar 

  16. Gantzer, C. J., Rittmann, B. E. & Herricks, E. E. Mass transport of biodegradable materials to streambed biofilms. Water Res. 22, 709–723 (1988)

    Article  CAS  Google Scholar 

  17. Kaplan, L. A. & Newbold, J. D. in Aquatic Ecosystems Interactivity of Dissolved Organic Matter (eds Findlay, S. E. G., & Sinsabaugh, R. L.) 97–119 (Academic, San Diego, London, 2003)

    Book  Google Scholar 

  18. Picioreanu, C., Van Loosdrecht, M. C. M. & Heijnen, J. J. A theoretical study on the effect of surface roughness on mass transport and transformation in biofilms. Biotechnol. Bioeng. 68, 355–369 (2000)

    Article  CAS  Google Scholar 

  19. Yang, X. M., Beyenal, H., Harkin, G. & Lewandowski, Z. Quantifying biofilm structure using image analysis. J. Microbiol. Methods 39, 109–119 (2000)

    Article  CAS  Google Scholar 

  20. Battin, T. J., Kaplan, L. A., Newbold, J. D., Cheng, X. & Hansen, C. Effects of current velocity on the nascent architecture of stream microbial biofilms. Appl. Environ. Microbiol. 69, 5443–5452 (2003)

    Article  CAS  Google Scholar 

  21. Lawrence, J. R., Neu, T. R. & Swerhorne, G. D. H. Application of multiple parameter imaging for the quantification of algae, bacterial, and exopolymer components of microbial biofilms. J. Microbiol. Methods 32, 253–261 (1998)

    Article  CAS  Google Scholar 

  22. Runkle, R. L. One-Dimensional Transport with Inflow and Storage (Otis): A Solute Transport Model for Streams and Rivers. Water-Resources Investigations Report 98–4018 (US Geological Survey, Denver, 1998)

    Google Scholar 

  23. Cheng, X. & Kaplan, L. A. Improved analysis of dissolved carbohydrates in stream water with HPLC-PAD. Anal. Chem. 73, 458–461 (2001)

    Article  CAS  Google Scholar 

  24. Newbold, J. D., Elwood, J. W., O'Neill, R. V. & Van Winkle, W. Measuring nutrient spiraling in streams. Can. J. Fish. Aquat. Sci. 38, 860–863 (1981)

    Article  Google Scholar 

Download references

Acknowledgements

We thank T. Georgian for insights regarding experimental design and the influence of biofilms on particle deposition; S. Roberts, M. Gentile and X. Cheng for technical assistance; K. Czymmek for CLSM support; and A. I. Packman, R. Sommaruga, G. Singer and J. Blaine for critically reading the manuscript. This work was supported by grants from the Austrian FWF (T.J.B.), the US NSF (L.A.K. and J.D.N.) and the Pennswood Fund for Environmental Research (L.A.K. and J.D.N.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tom J. Battin.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Battin, T., Kaplan, L., Denis Newbold, J. et al. Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426, 439–442 (2003). https://doi.org/10.1038/nature02152

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02152

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing