Birth weight and in-feed antibiotics alter the assembly and succession of the swine gut microbiota

Abstract

Understanding the principles of gut microbiota assembly and succession during host development is critical for effective gut microbiome manipulation to optimize host health and growth. The objective of this study was to conduct a high-frequency sampling of the swine gut microbiota from controlled groups of pigs to increase understanding of the dynamics of microbial community development. Here, a total of 924 fecal samples from 44 piglets (22 low-birth-weight, LBW; 22 normal-birth-weight, NBW) over 21 time points (1-41 days of age) collected every two days. Community composition, assembly, and succession was determined using 16S rRNA gene amplicon sequencing. Alpha diversity continuously increased during the suckling stage, yet no significant increase was observed during the days post-weaning. Post-weaning in-feed antibiotics consistently decreased microbial diversity and changed the community structure in both LBW and normal birth weight (NBW) piglets. Delayed post-weaning gut microbial community maturation was observed in LBW piglets compared with NBW. Heterogeneity of the gut microbial community between piglets linearly decreased over time, as revealed by the within-time Bray-Curtis dissimilarities. Individuality analysis on the relatively stable stage revealed that the gut microbiota composition of some individuals over time, and the abundance of most genera between individuals, were highly variable. Dirichlet multinomial mixtures analysis supported an age-dependent microbiota developmental pattern and identified the age-discriminatory taxa. The importance of stochastic processes in microbial community assembly increased over time within primary and secondary successions, despite the fact that the most dominant factors influencing community assembly were homogeneous selection and dispersal limitation, which are deterministic. IMPORTANCEOur understanding of the assembly and succession of the swine gut microbial community is limited, and scientific advancement in this interdisciplinary topic is hampered by individuality and transient dynamics. The solution to the above foundational questions is not only ecologically relevant but also useful for practical swine production. Our study addresses ecological processes shaping the swine gut microbiota between piglets with contrasting birth weights and receiving post-weaning antibiotics. Persistent gut microbiota immaturity in LBW piglets suggests that efforts to accelerate microbial community succession might improve LBW piglet growth performance and disease resistance. Intra-individual variance both in community structure and genus abundance during the post-weaning period indicates the importance of repeated measurements for reliable observations. Additionally, neutral (stochastic) processes increased as a factor of community assembly within each stage of pig growth, indicating that early intervention and multiple follow ups may be critical in manipulating the gut microbiota development.