Enterosignatures define common bacterial guilds in the human gut microbiome

Frioux, Clémence, Ansorge, Rebecca, Özkurt, Ezgi, Ghassemi Nedjad, Chabname, Fritscher, Joachim, Quince, Christopher, Waszak, Sebastian M. and Hildebrand, Falk (2023) Enterosignatures define common bacterial guilds in the human gut microbiome. Cell Host and Microbe, 31 (7). 1111-1125.e6. ISSN 1931-3128

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Abstract

The human gut microbiome composition is generally in a stable dynamic equilibrium, but it can deteriorate into dysbiotic states detrimental to host health. To disentangle the inherent complexity and capture the ecological spectrum of microbiome variability, we used 5,230 gut metagenomes to characterize signatures of bacteria commonly co-occurring, termed enterosignatures (ESs). We find five generalizable ESs dominated by either Bacteroides, Firmicutes, Prevotella, Bifidobacterium, or Escherichia. This model confirms key ecological characteristics known from previous enterotype concepts, while enabling the detection of gradual shifts in community structures. Temporal analysis implies that the Bacteroides-associated ES is “core” in the resilience of westernized gut microbiomes, while combinations with other ESs often complement the functional spectrum. The model reliably detects atypical gut microbiomes correlated with adverse host health conditions and/or the presence of pathobionts. ESs provide an interpretable and generic model that enables an intuitive characterization of gut microbiome composition in health and disease.

Item Type: Article
Additional Information: Data and code availability: This paper analyses existing, publicly available data. These accession numbers for the datasets are listed in the key resources table. All original code and additional datasets and results have been deposited at Zenodo and are publicly available as of the date of publication. The DOIs are listed in the key resources table and the content is further available in the following repository: https://gitlab.inria.fr/cfrioux/enterosignature-paper. Any additional information required to reanalyse the data reported in this paper is available from the lead contact upon request. Funding Information: R.A. E.O. and F.H. were supported by European Research Council H2020 StG (erc-stg-948219, EPYC). C.F. R.A. E.O. and F.H. were supported by the Biotechnology and Biological Sciences Research Council (BBSRC) Institute Strategic Programme Food Microbiome and Health BB/X011054/1 and its constituent project BBS/E/F/000PR13631, Gut Microbes and Health BB/r012490/1 and its constituent project BBS/e/F/000Pr10355, Core Capability Grant BB/CCG1720/1 and the work delivered via the Scientific Computing group, as well as support for the physical HPC infrastructure and data centre delivered via the NBI Computing infrastructure for Science (CiS) group. J.F. was supported by the UKRI Biotechnology and Biological Sciences Research Council Norwich Research Park Biosciences Doctoral Training Partnership BB/T008717/1. Some experiments presented in this paper were carried out using the PlaFRIM experimental testbed, supported by Inria, CNRS (LABRI and IMB), Université de Bordeaux, Bordeaux INP, and Conseil Régional d'Aquitaine (see https://www.plafrim.fr ). C.Q. was funded through the MRC Methodology grant “Strain resolved metagenomics for medical microbiology” MR/S037195/1. S.M.W. was supported by an SNSF Early Postdoc.Mobility Fellowship (P2ELP3_155365), an EMBO Long-Term Fellowship (ALTF 755-2014), and grants from the Research Council of Norway (187615), University of Oslo, and South-Eastern Norway Regional Health Authority. F.H. would like to thank Peer Bork and Jeroen Raes for insightful discussions on enterotypes. The authors thank Judith Pell for proofreading the article and all members of the Hildebrand group for valuable feedback, discussion, and support. We further want to thank the three anonymous reviewers for helping us in making the analysis more robust and impactful. Conceptualization: F.H. S.M.W. and C.F.; methodology: C.F. S.M.W. and C.Q.; software: C.F. F.H. J.F. R.A. and S.M.W.; validation: C.F.; formal analysis: C.F. R.A. and F.H.; investigation: C.F. R.A. F.H. and S.M.W.; data curation: C.F. F.H. E.Ö. R.A. and C.G.N.; writing – original draft: C.F. and F.H.; writing – review & editing: F.H. C.F. R.A. E.Ö. S.M.W. and C.Q. with contributions from all authors; visualization: C.F. F.H. S.M.W. and R.A.; supervision, project administration, and funding acquisition: F.H. The authors declare no competing interests. We support inclusive, diverse, and equitable conduct of research.
Uncontrolled Keywords: dysbiosis,enterosignatures,enterotypes,human gut microbiome,metagenomics,non-negative matrix factorization,parasitology,microbiology,virology,sdg 3 - good health and well-being ,/dk/atira/pure/subjectarea/asjc/2400/2405
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 31 Oct 2024 11:30
Last Modified: 01 Nov 2024 12:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/97363
DOI: 10.1016/j.chom.2023.05.024

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