Functional gut microbiota dynamics of generalist and specialist bacteria in association with chicken growth

Abstract The early-life development of the gut microbiome in broiler chickens is a dynamic ecological process with significant implications for host physiology and productivity. Using 388 genome-resolved metagenomic and 61 metatranscriptomic samples across two replicated trials, we analysed the compositional and functional succession of the caecal microbiome in chickens from hatching to slaughter age. We reconstructed 822 bacterial genomes and distilled gene annotations into comprehensive metabolic traits that captured the functional capacities of each genome. We observed that the increase in microbial diversity with chicken age was accompanied by a decline in community-level average metabolic capacity, driven by a shift from metabolically versatile generalists (Lachnospiraceae) to hitherto uncultured, genome-reduced specialists (RF39, RF32, and UBA1242). However, the specific identity of the dominant genome-reduced specialists varied among individuals, resulting in contrasting associations with host body weight. At slaughter age, only 10 UBA660 (RF39) bacteria were positively associated with body weight, while other genome-reduced lineages, such as UBA1242 (Christensenellales), were among 190 negatively associated bacteria. Gene expression analyses revealed that despite their reduced functional repertoire, UBA660 exhibited greater metabolic activity than UBA1242, particularly in the production of two key metabolites for host nutrition and intestinal homeostasis: the essential amino acid lysine and the signalling molecule indole-3-acetate. These findings provide new insights into the functional ecology of the chicken gut microbiome and highlight the relevance of cultivation approaches to retrieve underexplored and uncultured bacterial taxa, which could open new avenues for microbiome-based strategies aimed at improving poultry growth and health in intensive production systems.