Article

Species–function relationships shape ecological properties of the human gut microbiome

  • Nature Microbiology 1, Article number: 16088 (2016)
  • doi:10.1038/nmicrobiol.2016.88
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Abstract

Despite recent progress, the organization and ecological properties of the intestinal microbial ecosystem remain under-investigated. Here, using a manually curated metabolic module framework for (meta-)genomic data analysis, we studied species–function relationships in gut microbial genomes and microbiomes. Half of gut-associated species were found to be generalists regarding overall substrate preference, but we observed significant genus-level metabolic diversification linked to bacterial life strategies. Within each genus, metabolic consistency varied significantly, being low in Firmicutes genera and higher in Bacteroides. Differentiation of fermentable substrate degradation potential contributed to metagenomic functional repertoire variation between individuals, with different enterotypes showing distinct saccharolytic/proteolytic/lipolytic profiles. Finally, we found that module-derived functional redundancy was reduced in the low-richness Bacteroides enterotype, potentially indicating a decreased resilience to perturbation, in line with its frequent association to dysbiosis. These results provide insights into the complex structure of gut microbiome-encoded metabolic properties and emphasize the importance of functional and ecological assessment of gut microbiome variation in clinical studies.

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Acknowledgements

This research was funded by FP7 METACARDIS HEALTH-F4-2012- 305312 and IWT-SBO 100016. S.V.S. is funded by Marie Curie Actions FP7 People COFUND Proposal 267139 (acronym OMICS@VIB) and the Fund for Scientific Research-Flanders (FWO-V). S.C., M.V.C. and G.L.M. are funded by FWO-V. D.V. is funded by the Agency for Innovation by Science and Technology (IWT). The authors thank Dr Greenblum and collaborators and Dr Korem and collaborators for providing data.

Author information

Author notes

    • Sara Vieira-Silva
    •  & Gwen Falony

    These authors contributed equally to this work.

Affiliations

  1. Department of Microbiology and Immunology, KU Leuven–University of Leuven, Rega Institute, Herestraat 49, B-3000 Leuven, Belgium

    • Sara Vieira-Silva
    • , Gwen Falony
    • , Youssef Darzi
    • , Gipsi Lima-Mendez
    • , Doris Vandeputte
    • , Mireia Valles-Colomer
    • , Samuel Chaffron
    •  & Jeroen Raes
  2. VIB, Center for the Biology of Disease, Herestraat 49, B-3000 Leuven, Belgium

    • Sara Vieira-Silva
    • , Gwen Falony
    • , Youssef Darzi
    • , Gipsi Lima-Mendez
    • , Roberto Garcia Yunta
    • , Doris Vandeputte
    • , Mireia Valles-Colomer
    • , Falk Hildebrand
    • , Samuel Chaffron
    •  & Jeroen Raes
  3. Microbiology Unit, Faculty of Sciences and Bioengineering Sciences, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium

    • Youssef Darzi
    • , Gipsi Lima-Mendez
    • , Roberto Garcia Yunta
    • , Doris Vandeputte
    • , Falk Hildebrand
    • , Samuel Chaffron
    •  & Jeroen Raes
  4. Niigata University Graduate School of Medical and Dental Sciences 1-757 Asahimachi-dori, Chuo-ku, Niigata 951-8510, Japan

    • Shujiro Okuda

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Contributions

S.V.S. and G.F. contributed equally to this work. S.V.S. and G.F. designed the study, collected and processed data, performed the analyses and wrote the paper. G.F., S.V.S., D.V., M.V.C. and Y.D. curated the gut-specific metabolic modules. J.R. designed the study and co-wrote the paper. Y.D., R.G.Y., F.H. and S.O. participated in data collection and processing. G.L.M., Y.D., R.G.Y., S.O., D.V. and S.C. participated in statistical analyses. Y.D. participated in graphical representation design.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jeroen Raes.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1–9, Supplementary Data legends 1–3, Supplementary Table legends 1–11.

Text files

  1. 1.

    Supplementary Data 1

    Gut-specific metabolic modules formatted for easy integration into bioinformatics pipelines

  2. 2.

    Supplementary Data 2

    Gut reference genomes phylogenetic tree

Excel files

  1. 1.

    Supplementary Information

    Supplementary Tables 1–11