Bioactive glycans in a microbiome-directed food for children with malnutrition

Matthew C. Hibberd, Daniel M. Webber, Dmitry A. Rodionov, Suzanne Henrissat, Robert Y. Chen, Cyrus Zhou, Hannah M. Lynn, Yi Wang, Hao-Wei Chang, Evan M. Lee, Janaki Lelwala-Guruge, Marat D. Kazanov, Aleksandr A. Arzamasov, Semen A. Leyn, Vincent Lombard, Nicolas Terrapon, Bernard Henrissat, Juan J. Castillo, Garret Couture, Nikita P. Bacalzo, Ye Chen, Carlito B. Lebrilla, Ishita Mostafa, Subhasish Das, Mustafa Mahfuz, Michael J. Barratt, Andrei L. Osterman, Tahmeed Ahmed and Jeffrey I. Gordon ()
Additional contact information
Matthew C. Hibberd: Washington University School of Medicine
Daniel M. Webber: Washington University School of Medicine
Dmitry A. Rodionov: Sanford Burnham Prebys Medical Discovery Institute
Suzanne Henrissat: Washington University School of Medicine
Robert Y. Chen: Washington University School of Medicine
Cyrus Zhou: Washington University School of Medicine
Hannah M. Lynn: Washington University School of Medicine
Yi Wang: Washington University School of Medicine
Hao-Wei Chang: Washington University School of Medicine
Evan M. Lee: Washington University School of Medicine
Janaki Lelwala-Guruge: Washington University School of Medicine
Marat D. Kazanov: Sabanci University
Aleksandr A. Arzamasov: Sanford Burnham Prebys Medical Discovery Institute
Semen A. Leyn: Sanford Burnham Prebys Medical Discovery Institute
Vincent Lombard: CNRS, Aix-Marseille University
Nicolas Terrapon: CNRS, Aix-Marseille University
Bernard Henrissat: Technical University of Denmark
Juan J. Castillo: University of California, Davis
Garret Couture: University of California, Davis
Nikita P. Bacalzo: University of California, Davis
Ye Chen: Washington University School of Medicine
Carlito B. Lebrilla: University of California, Davis
Ishita Mostafa: International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b)
Subhasish Das: International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b)
Mustafa Mahfuz: International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b)
Michael J. Barratt: Washington University School of Medicine
Andrei L. Osterman: Sanford Burnham Prebys Medical Discovery Institute
Tahmeed Ahmed: International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b)
Jeffrey I. Gordon: Washington University School of Medicine

Nature, 2024, vol. 625, issue 7993, 157-165

Abstract: Abstract Evidence is accumulating that perturbed postnatal development of the gut microbiome contributes to childhood malnutrition1–4. Here we analyse biospecimens from a randomized, controlled trial of a microbiome-directed complementary food (MDCF-2) that produced superior rates of weight gain compared with a calorically more dense conventional ready-to-use supplementary food in 12–18-month-old Bangladeshi children with moderate acute malnutrition4. We reconstructed 1,000 bacterial genomes (metagenome-assembled genomes (MAGs)) from the faecal microbiomes of trial participants, identified 75 MAGs of which the abundances were positively associated with ponderal growth (change in weight-for-length Z score (WLZ)), characterized changes in MAG gene expression as a function of treatment type and WLZ response, and quantified carbohydrate structures in MDCF-2 and faeces. The results reveal that two Prevotella copri MAGs that are positively associated with WLZ are the principal contributors to MDCF-2-induced expression of metabolic pathways involved in utilizing the component glycans of MDCF-2. The predicted specificities of carbohydrate-active enzymes expressed by their polysaccharide-utilization loci are correlated with (1) the in vitro growth of Bangladeshi P. copri strains, possessing varying degrees of polysaccharide-utilization loci and genomic conservation with these MAGs, in defined medium containing different purified glycans representative of those in MDCF-2, and (2) the levels of faecal carbohydrate structures in the trial participants. These associations suggest that identifying bioactive glycan structures in MDCFs metabolized by growth-associated bacterial taxa will help to guide recommendations about their use in children with acute malnutrition and enable the development of additional formulations.

Date: 2024
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DOI: 10.1038/s41586-023-06838-3

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