Stochasticity Highlights the Development of Both the Gastrointestinal and Upper-Respiratory-Tract Microbiomes of Neonatal Dairy Calves in Early Life.

Simple Summary: Many factors influence the development and establishment of the neonatal gut and upper-respiratory-tract microbiomes. Importantly, these microbiomes play a significant role in host maintenance and health physiologies in host–microbe systems. In dairy calf systems, the ecological factors impacting microbial assembly are not fully elucidated. Thus, the aim of this pilot study was to characterize the establishment of early-life fecal and nasal microbiomes in dairy calves and evaluate the impact of disease states on microbial development. In addition, we investigated the governing forces of microbial composition to better understand the factors that shape microbial community populations. Herein, we observed dynamic changes in diversity and composition in the neonatal calf microbiomes and demonstrated that disease state impacts the gastrointestinal microbiome. Our results further suggest that early-life microbiomes are stochastically driven, governed by neutral theory-based dynamics. These results together provide researchers with a roadmap to further investigate how early-life microbiomes develop and how they are affected by disease. Together, this study and future studies could help improve the quality of life in dairy calf management. The microbiome of dairy calves undergoes extensive change due to various forces during the first weeks of life. Importantly, diseases such as bovine respiratory disease (BRD) and calf diarrhea can have profound impacts on the early-life microbiome. Therefore, a longitudinal, repeated-measures pilot study was designed to characterize the establishment of nasal and fecal microbiomes of dairy calves, assess the governing forces of microbial assembly, and evaluate how disease states impact these microbial ecologies. Dairy calves (n = 19) were clinically evaluated for gastrointestinal and respiratory disease across three weeks beginning at age ≤ seven days old. Fecal (n = 57) and nasal (n = 57) microbial samples were taken for paired-end 16S rRNA gene amplicon sequencing. Taxonomy and diversity analyses were used to characterize early-life nasal and fecal microbiomes. Stochasticity and determinism were measured using normalized stochasticity testing (NST) and Dirichlet multinomial model (DMM). All analyses were tested for statistical significance. Clinical diarrhea was observed in 11 of the 19 calves. Clinical BRD was not independently observed among the cohort; however, two calves presented clinical signs of both BRD and diarrhea. Taxonomic analysis revealed that fecal samples were highlighted by Bacteroidaceae (40%; relative abundance), Ruminococcaceae (13%), and Lachnospiraceae (10%), with changes in diversity (Kruskal–Wallis; p < 0.05) and composition (PERMANOVA; p < 0.05). Clinical diarrhea reduced diversity in the fecal microbiome but did not impact composition. Nasal samples featured Moraxellaceae (49%), Mycoplasmataceae (16%), and Pasteurellaceae (3%). While no diversity changes were seen in nasal samples, compositional changes were observed (p < 0.05). NST metrics (Kruskal–Wallis; p > 0.01) and DMM (PERMANOVA; p < 0.01) revealed that stochastic, neutral theory-based assembly dynamics govern early-life microbial composition and that distinct microbial populations drive community composition in healthy and diarrheic calves. [ABSTRACT FROM AUTHOR]