Topological characteristics and longitudinal dynamics of co-abundance networks involving beneficial commensal bacteria in the pig gut microbiome and its association with average daily gain

Microorganisms are intricately interrelated with each other in the gut microecosystem, which influences the colonization and functional roles of probiotics. However, how these interactions dynamically change during host development and whether their topological features influence host phenotypes, such as average daily gain (ADG), remain poorly understood. In this study, we performed metagenome analysis for 2,311 fecal samples collected from a specifically designed eight genetically divergent breed intercrossed mosaic F6 and F7 population, at three developmental ages of 25 days (D25), 120 days (D120), and 240 days (D240) of each individual, covering pre-weaning to market. By constructing their microbiota co-abundance networks, we systematically characterized dynamic changes in beneficial commensal bacteria involved co-abundance networks in the pig gut microbiome across three ages. We elucidated conserved and variable co-abundance features involving these bacteria across developmental stages. We observed that the cross-age stable co-abundance correlations of beneficial commensal bacteria were maintained by a large set of weak correlations. A subset of age-shared co-abundance correlations remained variable across different ages in correlation strength and direction. Topological analysis revealed that beneficial commensal bacteria involved co-abundance networks were highly age-specific. Among the three age stages sampled in this study, the D120 stage represented a critical window for the structural and functional reorganization of gut microbiota. Using metagenomic sequencing data at the D120, we identified two guilds that were significantly associated with ADG from D120 to D240. Guild 1 included short chain fatty acid-producing taxa and was positively associated with ADG, whereas Guild 2 tended to self-utilization of energy and was negatively associated with ADG. We also inferred the ecological interaction mechanisms of ADG-associated microbial communities using genome-scale metabolic models. These findings provided a theoretical basis for stage-specific intervention in the pig gut microbiome using probiotics to improve production traits.