Metabolic modeling of microbial communities in the chicken ceca reveals a landscape of competition and co-operation

Members of the Bacteroidales, particularly Bacteroides species, with their ability to degrade dietary fibers and liberate otherwise unavailable substrates, exert a substantial influence on the microbiome of the lower intestine. However, our understanding of how this influence translates to the metabolic interactions that support community structure remains limited. In this study, we apply constraint-based modeling to investigate metabolic interactions in chicken cecal communities categorized by the presence or absence of Bacteroides.

From metagenomic datasets previously generated from 33 chicken ceca, we constructed 237 metagenome-assembled genomes. Metabolic modeling of communities built from these genomes generated profiles of short-chain fatty acids largely consistent with experimental assays and confirmed the role of B. fragilis as a metabolic hub, central to the production of metabolites consumed by other taxa. In its absence, communities undergo significant functional reconfiguration, with metabolic roles typically fulfilled by B. fragilis assumed by multiple taxa. Beyond B. fragilis, we found Escherichia coli and Lactobacillus crispatus also mediate influential metabolic roles, which vary in the presence or absence of B. fragilis. Notably, the microbiome's compensatory adaptations in the absence of B. fragilis produced metabolic alterations resembling those previously associated with inflammatory bowel disease in humans, including energy deficiency, increased lactate production, and altered amino acid metabolism.

This work demonstrates the potential of using the chicken cecal microbiome as a model system for investigating the complex metabolic interactions and key contributions that drive community dynamics in the gut. Our model-based predictions offer insights into how keystone taxa like B. fragilis may shape the metabolic landscape and functional organization of microbial communities. The observed metabolic adaptations in the absence of B. fragilis share metabolic similarities with profiles seen in dysbiotic states in humans and underscore the translational relevance of these insights for understanding gut health across different host systems. Video Abstract.