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Nutritional preferences of human gut bacteria reveal their metabolic idiosyncrasies

Nature Microbiology volume 3, pages 514–522 (2018)Cite this article

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Abstract

Bacterial metabolism plays a fundamental role in gut microbiota ecology and host–microbiome interactions. Yet the metabolic capabilities of most gut bacteria have remained unknown. Here we report growth characteristics of 96 phylogenetically diverse gut bacterial strains across 4 rich and 15 defined media. The vast majority of strains (76) grow in at least one defined medium, enabling accurate assessment of their biosynthetic capabilities. These do not necessarily match phylogenetic similarity, thus indicating a complex evolution of nutritional preferences. We identify mucin utilizers and species inhibited by amino acids and short-chain fatty acids. Our analysis also uncovers media for in vitro studies wherein growth capacity correlates well with in vivo abundance. Further value of the underlying resource is demonstrated by correcting pathway gaps in available genome-scale metabolic models of gut microorganisms. Together, the media resource and the extracted knowledge on growth abilities widen experimental and computational access to the gut microbiota.

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Fig. 1: Species and media selection.
Fig. 2: Growth profiles of 96 gut bacterial strains across 19 media.
Fig. 3: Species growth patterns provide insights into microbiota ecology.
Fig. 4: Selected metabolic characteristics of gut bacteria revealed by our screen.
Fig. 5: Defined media resource improves genome-scale metabolic models of gut bacteria.

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Acknowledgements

We thank H. KleinJan and L. Maier for experimental assistance, O. Ponomarova for advice on media design and D. Machado for advice on metabolic modelling. Sequencing was performed at Genecore, EMBL. We thank Dupont Health and Nutrition (formerly Danisco Sweeteners OY, Finland) for providing L. acidophilus NCFM, L. paracasei ATCC SDS275, B. animalis subsp. lactis Bl-04 and BI-07, D. Clarke for Shigella sonnei 53 G and the enteropathogenic Escherichia coli strains CFT073, E2348/69, H10407, HM605 and UTI89, E. Denamur for the Escherichia coli strains ED1a and IAI1, M. Blokesch for the Vibrio cholerae strains A1552 and N16961, H. Andrews-Polymenis for the Salmonella enterica typhimurium strains CDC 6516-60 and LT2 and C. Darby for Yersinia pseudotuberculosis YPIII. This project has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement no. 686070. MT and MP were supported by the EMBL interdisciplinary postdoctoral program.

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Author notes

  1. Mihaela Pruteanu

    Present address: Humboldt University Berlin, Berlin, Germany

  2. Aleksej Zelezniak

    Present address: Chalmers University of Technology, Gothenburg, Sweden

  3. These authors contributed equally: Melanie Tramontano and Sergej Andrejev.

Authors and Affiliations

  1. European Molecular Biology Laboratory, Heidelberg, Germany

    Melanie Tramontano, Sergej Andrejev, Mihaela Pruteanu, Martina Klünemann, Michael Kuhn, Paula Jouhten, Aleksej Zelezniak, Georg Zeller, Peer Bork, Athanasios Typas & Kiran Raosaheb Patil

  2. EMBL-EBI, Wellcome Trust Genome Campus, Cambridge, United Kingdom

    Marco Galardini

  3. Max-Delbrück-Centre for Molecular Medicine, Berlin, Germany

    Peer Bork

  4. Molecular Medicine Partnership Unit, Heidelberg, Germany

    Peer Bork

  5. Department of Bioinformatics, Biocenter, University of Würzburg, Würzburg, Germany

    Peer Bork

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Contributions

M.T., P.B., A.T. and K.R.P. conceived the study. M.T., S.A., A.T. and K.R.P. designed the study. M.T., M.P., A.Z. and G.Z. selected gut bacterial strains. M.T. and M.Klünemann performed in vitro experiments. S.A. analysed data. S.A. and P.J. performed metabolic modelling. S.A. and G.Z. compiled figures. M.Kuhn contributed to in vivo abundance analysis. M.G. annotated sequenced genomes. P.B., A.T. and K.R.P. supervised the study. M.T., S.A. and K.R.P. wrote the manuscript. All authors read and commented on the manuscript.

Corresponding authors

Correspondence to Peer Bork, Athanasios Typas or Kiran Raosaheb Patil.

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Tramontano, M., Andrejev, S., Pruteanu, M. et al. Nutritional preferences of human gut bacteria reveal their metabolic idiosyncrasies. Nat Microbiol 3, 514–522 (2018). https://doi.org/10.1038/s41564-018-0123-9

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