Drivers and determinants of strain dynamics following fecal microbiota transplantation

Drivers and determinants of strain dynamics following fecal microbiota transplantation

Fecal microbiota transplantation (FMT) is a therapeutic intervention for inflammatory diseases of the gastrointestinal tract, but its clinical mode of action and subsequent microbiome dynamics remain poorly understood. Here we analyzed metagenomes from 316 FMTs, sampled pre and post intervention, fo...

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Published in:Nature medicine Vol. 28; no. 9; pp. 1902 - 1912
Main Authors: Schmidt, Thomas S. B., Li, Simone S., Maistrenko, Oleksandr M., Akanni, Wasiu, Coelho, Luis Pedro, Dolai, Sibasish, Fullam, Anthony, Glazek, Anna M., Hercog, Rajna, Herrema, Hilde, Jung, Ferris, Kandels, Stefanie, Orakov, Askarbek, Thielemann, Roman, von Stetten, Moritz, Van Rossum, Thea, Benes, Vladimir, Borody, Thomas J., de Vos, Willem M., Ponsioen, Cyriel Y., Nieuwdorp, Max, Bork, Peer
Format: Journal Article
Language:English
Published: New York Nature Publishing Group US 01-09-2022
Nature Publishing Group
Subjects:
631/326/2565/107
631/326/2565/2134
631/326/2565/2142
631/326/2565/855
Biomedical and Life Sciences
Biomedicine
Cancer Research
Clinical outcomes
Colonization
Complementarity
Dynamics
Fecal microflora
Feces
Gastrointestinal system
Gastrointestinal tract
Genomes
Infectious Diseases
Inflammatory diseases
Intestinal microflora
Metabolic Diseases
Microbial activity
Microbiomes
Microbiota
Microorganisms
Mode of action
Molecular Medicine
Neurosciences
Population dynamics
Regression analysis
Regression models
Stratification
Transplantation
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Summary:Fecal microbiota transplantation (FMT) is a therapeutic intervention for inflammatory diseases of the gastrointestinal tract, but its clinical mode of action and subsequent microbiome dynamics remain poorly understood. Here we analyzed metagenomes from 316 FMTs, sampled pre and post intervention, for the treatment of ten different disease indications. We quantified strain-level dynamics of 1,089 microbial species, complemented by 47,548 newly constructed metagenome-assembled genomes. Donor strain colonization and recipient strain resilience were mostly independent of clinical outcomes, but accurately predictable using LASSO-regularized regression models that accounted for host, microbiome and procedural variables. Recipient factors and donor–recipient complementarity, encompassing entire microbial communities to individual strains, were the main determinants of strain population dynamics, providing insights into the underlying processes that shape the post-FMT gut microbiome. Applying an ecology-based framework to our findings indicated parameters that may inform the development of more effective, targeted microbiome therapies in the future, and suggested how patient stratification can be used to enhance donor microbiota colonization or the displacement of recipient microbes in clinical practice. Understanding the factors underlying colonization of donor microbes in recipients of fecal microbiota transplantation is a necessary first step to aid development of directed approaches that aim to couple colonization to clinical outcomes.
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ISSN:1078-8956
1546-170X
DOI:10.1038/s41591-022-01913-0