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Attached biofilms and suspended aggregates are distinct microbial lifestyles emanating from differing hydraulics

Abstract

Small-scale hydraulics affects microbial behaviour at the cell level1, trophic interactions in marine aggregates2 and the physical structure and function of stream biofilms3,4. However, it remains unclear how hydraulics, predictably changing from small streams to large rivers, impacts the structure and biodiversity of complex microbial communities in these ecosystems. Here, we present experimental evidence unveiling hydraulics as a hitherto poorly recognized control of microbial lifestyle differentiation in fluvial ecosystems. Exposing planktonic source communities from stream and floodplain ecosystems to different hydraulic environments revealed strong selective hydraulic pressures but only minor founder effects on the differentiation of attached biofilms and suspended aggregates and their biodiversity dynamics. Key taxa with a coherent phylogenetic underpinning drove this differentiation. Only a few resident and phylogenetically related taxa formed the backbone of biofilm communities, whereas numerous resident taxa characterized aggregate communities. Our findings unveil fundamental differences between biofilms and aggregates and build the basis for a mechanistic understanding of how hydraulics drives the distribution of microbial diversity along the fluvial continuum57.

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Figure 1: Temporal patterns of biodiversity in suspended aggregates and biofilms.
Figure 2: Community composition and dynamics of microbial lifestyles.
Figure 3: Phylogenetic distance and co-occurrence of attached biofilms and suspended aggregates.
Figure 4: Temporal dynamics of resident and transient core populations and of conditionally rare taxa in attached biofilms and suspended aggregates.

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References

  1. Guasto, J. S., Rusconi, R. & Stocker, R. Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 44, 373–400 (2012).

    Article  Google Scholar 

  2. Stocker, R. Marine microbes see a sea of gradients. Science 338, 628–633 (2012).

    Article  CAS  Google Scholar 

  3. Battin, T. J., Kaplan, L. A., Denis Newbold, J. & Hansen, C. M. E. Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426, 439–442 (2003).

    Article  CAS  Google Scholar 

  4. Battin, T. J., Besemer, K., Bengtsson, M. M., Romaní, A. M. & Packmann, A. I. The ecology and biogeochemistry of stream biofilms. Nat. Rev. Microbiol. 14, 251–263 (2016).

    Article  CAS  Google Scholar 

  5. Read, D. S. et al. Catchment-scale biogeography of riverine bacterioplankton. ISME J. 9, 516–526 (2014).

    Article  Google Scholar 

  6. Besemer, K. et al. Headwaters are critical reservoirs of microbial diversity for fluvial networks. Proc. R. Soc. B 280, 20131760 (2013).

    Article  Google Scholar 

  7. Savio, D. et al. Bacterial diversity along a 2600 km river continuum. Environ. Microbiol. 17, 4994–5007 (2015).

    Article  CAS  Google Scholar 

  8. Battin, T. J. et al. Biophysical controls on organic carbon fluxes in fluvial networks. Nat. Geosci. 1, 95–100 (2008).

    Article  CAS  Google Scholar 

  9. Klappenbach, J. A., Dunbar, J. M. & Schmidt, T. M. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66, 1328–1333 (2000).

    Article  CAS  Google Scholar 

  10. Nemergut, D. R. et al. Decreases in average bacterial community rRNA operon copy number during succession. ISME J. 10, 1147–1156 (2016).

    Article  CAS  Google Scholar 

  11. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108 (2004).

    Article  CAS  Google Scholar 

  12. Augspurger, C., Karwautz, C., Mußmann, M., Daims, H. & Battin, T. J. Drivers of bacterial colonization patterns in stream biofilms. FEMS Microbiol. Ecol. 72, 47–57 (2010).

    Article  CAS  Google Scholar 

  13. Smriga, S., Fernandez, V. I., Mitchell, J. G. & Stocker, R. Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc. Natl Acad. Sci. USA 113, 1576–1581 (2016).

    Article  CAS  Google Scholar 

  14. Simon, M., Grossart, H. P., Schweitzer, B. & Ploug, H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microbial Ecol. 28, 175–211 (2002).

    Article  Google Scholar 

  15. Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).

    Article  Google Scholar 

  16. Zeglin, L. H. Stream microbial diversity responds to environmental changes: review and synthesis of existing research. Front. Microbiol. 6, 454 (2015).

    Article  Google Scholar 

  17. Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D. & Bertilsson, S. A guide to the natural history of freshwater lake bacteria. Microbiol. Mol. Biol. Rev. 75, 14–49 (2011).

    Article  CAS  Google Scholar 

  18. Fernandez-Gomez, B. et al. Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J. 7, 1026–1037 (2013).

    Article  CAS  Google Scholar 

  19. Faust, K. et al. Microbial co-occurrence relationships in the human microbiome. PLoS Comput. Biol. 8, e1002606 (2012).

    Article  CAS  Google Scholar 

  20. Berry, D . & Widder, S. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front. Microbiol. 5, 219 (2014).

    Article  Google Scholar 

  21. Stewart, P. S. & Franklin, M. J. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6, 199–210 (2008).

    Article  CAS  Google Scholar 

  22. Langille, M. G. I. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821 (2013).

    Article  CAS  Google Scholar 

  23. Hansen, S. K., Rainey, P. B., Haagensen, J. A. J. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007).

    Article  CAS  Google Scholar 

  24. Wilmes, P. et al. Natural acidophilic biofilm communities reflect distinct organismal and functional organization. ISME J. 3, 266–270 (2009).

    Article  CAS  Google Scholar 

  25. Shade, A. et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio 5, e01371 (2014).

    Article  Google Scholar 

  26. Lynch, M. D. J. & Neufeld, J. D. Ecology and exploration of the rare biosphere. Nat. Rev. Microbiol. 13, 217–229 (2015).

    Article  CAS  Google Scholar 

  27. Wilhelm, L. et al. Rare but active taxa contribute to community dynamics of benthic biofilms in glacier-fed streams. Environ. Microbiol. 16, 2514–2524 (2014).

    Article  CAS  Google Scholar 

  28. Besemer, K. et al. Unraveling assembly of stream biofilm communities. ISME J. 6, 1459–1468 (2012).

    Article  CAS  Google Scholar 

  29. Singer, G. et al. Microcosm design and evaluation to study stream microbial biofilms. Limnol. Oceanogr. 4, 436–447 (2006).

    Article  Google Scholar 

  30. Urich, T. et al. Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3, e2527 (2008).

    Article  Google Scholar 

  31. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).

    Article  CAS  Google Scholar 

  32. Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120 (2013).

    Article  CAS  Google Scholar 

  33. Vegan: community ecology package v2.4-0 (Oksanen, J. et al., 2016).

  34. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Article  CAS  Google Scholar 

  35. Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).

    Article  CAS  Google Scholar 

  36. McMurdie, P. J. & Holmes, S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).

    Article  CAS  Google Scholar 

  37. Kahm, M., Hasenbrink, G., Lichtenberg-Fraté, H., Ludwig, J. & Kschischo, M. Grofit: fitting biological growth curves with R. J. Stat. Soft. 33, 1–21 (2010).

    Article  Google Scholar 

  38. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).

    Book  Google Scholar 

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Acknowledgements

The authors thank P. Pramateftaki and A. Gernand for assistance in the laboratory. Financial support was provided by the Austrian Science Fund (START Y420-B17) to T.J.B. and from internal funding from the Ecole Polytechnique Fédérale de Lausanne (EPFL) to R.N.

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Authors and Affiliations

Authors

Contributions

R.N. together with T.J.B., conceived and conducted the experiments and the analyses. R.N., together with H.P., conducted bioinformatical and statistical analyses. T.J.B. wrote the paper with help from R.N. and H.P.

Corresponding author

Correspondence to Tom J. Battin.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Figures 1–7, Supplementary Tables 1–2 (PDF 967 kb)

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Niederdorfer, R., Peter, H. & Battin, T. Attached biofilms and suspended aggregates are distinct microbial lifestyles emanating from differing hydraulics. Nat Microbiol 1, 16178 (2016). https://doi.org/10.1038/nmicrobiol.2016.178

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