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Evolution of species interactions in a biofilm community

Abstract

Biofilms are spatially structured communities of microbes whose function is dependent on a complex web of symbiotic interactions1,2. Localized interactions within these assemblages are predicted to affect the coexistence of the component species3,4,5, community structure6 and function7,8,9,10, but there have been few explicit empirical analyses of the evolution of interactions11. Here we show, with the use of a two-species community, that selection in a spatially structured environment leads to the evolution of an exploitative interaction. Simple mutations in the genome of one species caused it to adapt to the presence of the other, forming an intimate and specialized association. The derived community was more stable and more productive than the ancestral community. Our results show that evolution in a spatially structured environment can stabilize interactions between species, provoke marked changes in their symbiotic nature and affect community function.

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Figure 1: Coexistence of P. putida KT2440 and Acinetobacter sp. C6 in structured (biofilm flow chamber) and unstructured (chemostat) environments with benzyl alcohol as the sole carbon source.
Figure 2: Characteristic biofilm and colony phenotypes of the ancestral and the derived rough variant of P. putida.
Figure 3: Competitive fitness of the rough variant of P. putida.
Figure 4: Productivity of ancestral and derived communities.

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Acknowledgements

We thank T. Fukami, R. Kassen, D. Refardt, T. Cooper, T. Monds and T. Martini Jørgensen for comment and discussion. Grants from the Danish Research Councils to S.M. supported this work.

Author Contributions S.K.H., S.M. and P.B.R. designed the experiments; S.K.H. and J.A.J.H. conducted the experiments; S.K.H., S.M. and P.B.R. analysed the data and wrote the paper.

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Correspondence to Paul B. Rainey.

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Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Data, Supplementary Methods 1 and 2, Supplementary Table 1, Supplementary Figure 1 and Supplementary Notes. Supplementary Data details IFR experiments. Supplementary Methods 1 describe the mapping of spontaneous wapH mutants. Supplementary Table 1 lists the P. putida transposon mutants. Supplementary Methods 2 details the biofilm and chemostat experiments. Supplementary Figure 1 shows LPS profiles of various P. putida derivatives. Supplementary Notes contain references. (PDF 365 kb)

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Hansen, S., Rainey, P., Haagensen, J. et al. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007). https://doi.org/10.1038/nature05514

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