Integrative genomic reconstruction reveals heterogeneity in carbohydrate utilization across human gut bifidobacteria

2024 · doi:10.1101/2024.07.06.602360
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This study reconstructed carbohydrate utilization pathways in bifidobacteria from genomic data, revealing significant heterogeneity and identifying specific strains capable of metabolizing α-glucans, xyloglucan, and human milk oligosaccharides.

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The paper studied strain-level heterogeneity in carbohydrate utilization among human gut bifidobacteria by reconstructing 68 pathways for mono-, di-, oligo-, and polysaccharide metabolism from curated metabolic functional roles across 3,083 cultured Bifidobacterium isolates and human-origin metagenome-assembled genomes. It found extensive inter- and intraspecies variation, including a distinct clade within B. longum capable of metabolizing α-glucans and Bangladeshi-origin isolates with gene clusters for xyloglucan and human milk oligosaccharides breakdown, with 38 predicted carbohydrate utilization phenotypes validated in vitro using 30 geographically diverse isolates. The caveat is that pathway reconstruction and validation are limited to genomic content and in vitro growth experiments rather than direct measurement of carbohydrate utilization in living hosts. This paper does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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Abstract

Bifidobacteria are among the earliest colonizers of the human gut and are widely used as probiotics for their health-promoting properties. However, individual responses to probiotic supplementation may vary with strain type(s), microbiota composition, diet, or lifestyle conditions, highlighting the need for strain-level insights into the bifidobacterial metabolism of dietary and host glycans. Here, we systematically reconstructed 68 pathways involved in the utilization of mono-, di-, oligo-, and polysaccharides by analyzing the distribution of 589 curated metabolic functional roles (catabolic enzymes, transporters, transcriptional regulators) in 3083 non-redundant cultured Bifidobacterium isolates and metagenome-assembled genomes (MAGs) of human origin. Our analysis uncovered extensive inter- and intraspecies heterogeneity, including a distinct clade within the Bifidobacterium longum species capable of metabolizing α-glucans. We also identified isolates of Bangladeshi origin that harbor unique gene clusters implicated in the breakdown of xyloglucan and human milk oligosaccharides. Thirty-eight predicted carbohydrate utilization phenotypes were experimentally validated in 30 geographically diverse Bifidobacterium isolates in vitro. Our large-scale genomic compendium expands the knowledge of bifidobacterial carbohydrate metabolism and can inform the rational design of probiotic and synbiotic formulations tailored to strain-specific nutrient preferences.
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Abstract Bifidobacteria are among the earliest colonizers of the human gut and are widely used as probiotics for their health-promoting properties. However, individual responses to probiotic supplementation may vary with strain type(s), microbiota composition, diet, or lifestyle conditions, highlighting the need for strain-level insights into the bifidobacterial metabolism of dietary and host glycans. Here, we systematically reconstructed 68 pathways involved in the utilization of mono-, di-, oligo-, and polysaccharides by analyzing the distribution of 589 curated metabolic functional roles (catabolic enzymes, transporters, transcriptional regulators) in 3083 non-redundant cultured Bifidobacterium isolates and metagenome-assembled genomes (MAGs) of human origin. Our analysis uncovered extensive inter- and intraspecies heterogeneity, including a distinct clade within the Bifidobacterium longum species capable of metabolizing α-glucans. We also identified isolates of Bangladeshi origin that harbor unique gene clusters implicated in the breakdown of xyloglucan and human milk oligosaccharides. Thirty-eight predicted carbohydrate utilization phenotypes were experimentally validated in 30 geographically diverse Bifidobacterium isolates in vitro. Our large-scale genomic compendium expands the knowledge of bifidobacterial carbohydrate metabolism and can inform the rational design of probiotic and synbiotic formulations tailored to strain-specific nutrient preferences. Competing Interest Statement D.A.R. and A.L.O. are co-founders of Phenobiome Inc., a company pursuing the development of personalized nutritional solutions to balance the gut microbiome. L.B. is a coinventor on patent applications related to the use of HMOs in preventing necrotizing enterocolitis and other inflammatory diseases. The remaining authors of this paper declare no competing interests. Footnotes The manuscript has been substantially revised in response to the reviewers' comments.

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