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Surveys, simulation and single-cell assays relate function and phylogeny in a lake ecosystem

Nature Microbiology volume 1, Article number: 16130 (2016) Cite this article

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Abstract

Much remains unknown about what drives microbial community structure and diversity. Highly structured environments might offer clues. For example, it may be possible to identify metabolically similar species as groups of organisms that correlate spatially with the geochemical processes they carry out. Here, we use a 16S ribosomal RNA gene survey in a lake that has chemical gradients across its depth to identify groups of spatially correlated but phylogenetically diverse organisms. Some groups had distributions across depth that aligned with the distributions of metabolic processes predicted by a biogeochemical model, suggesting that these groups performed biogeochemical functions. A single-cell genetic assay showed, however, that the groups associated with one biogeochemical process, sulfate reduction, contained only a few organisms that have the genes required to reduce sulfate. These results raise the possibility that some of these spatially correlated groups are consortia of phylogenetically diverse and metabolically different microbes that cooperate to carry out geochemical functions.

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Figure 1: Bacterial survey of the lake identified communities that vary with depth.
Figure 2: The model creates a dynamic picture of chemical changes that occur in the lake through the lake's depth (vertical axis) across time (horizontal).
Figure 3: Distribution of key populations (black lines, relative abundance) from 2013 and their correspondence with modelled processes (red lines, relative rate).
Figure 4: Operational ecological units (OEUs) are composed of phylogenetically diverse OTUs that largely align with modelled processes.
Figure 5: OEUs corresponding to sulfate reduction do not have metabolically identical OTUs.

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Acknowledgements

This material is based on work supported by the National Science Foundation Graduate Research Fellowship (grant no. 1122374) and by the US Department of Energy, Office of Science, Office of Biological and Environmental Research (award no. DE-SC0008743).

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Author notes

  1. Sarah P. Preheim and Scott W. Olesen: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Sarah P. Preheim, Scott W. Olesen, Sarah J. Spencer & Eric J. Alm

  2. Department of Geography and Environmental Engineering, Johns Hopkins University, Baltimore, 21218, Maryland, USA

    Sarah P. Preheim

  3. Qiagen Corp., 8000 Aarhus, Denmark

    Arne Materna

  4. Lawrence Berkeley National Laboratory, Berkeley, 94720, California, USA

    Charuleka Varadharajan

  5. École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland

    Matthew Blackburn

  6. Department of Physics, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Jonathan Friedman

  7. Institute Centre for Water and Environment (iWater), Masdar Institute of Science and Technology, PO Box 54224, Abu Dhabi, United Arab Emirates

    Jorge Rodríguez

  8. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Harold Hemond

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Contributions

S.P.P., S.W.O., H.H. and E.J.A. designed the research. S.P.P., S.W.O., A.M., C.V., M.B. and S.J.S. performed the research. S.P.P., S.W.O., J.F. and J.R. contributed analytical tools. S.P.P., S.W.O. and J.R. analysed the data. S.P.P., S.W.O. and E.J.A. wrote the paper.

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Correspondence to Eric J. Alm.

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Preheim, S., Olesen, S., Spencer, S. et al. Surveys, simulation and single-cell assays relate function and phylogeny in a lake ecosystem. Nat Microbiol 1, 16130 (2016). https://doi.org/10.1038/nmicrobiol.2016.130

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