Maternal factors predetermine offspring development and health, including the establishment of offsprings' first microbiomes. Research in swine has shown that early microbial exposures impact microbiome colonization in piglets, but this phenomenon has never been tested in the context of delivery room disinfection. Thus, we exposed gestating sows to two delivery environments (n = 3/environment): stalls cleaned with a broad-spectrum disinfectant (disinfected environment [D]) or stalls cleaned only with hot-water power washing (nondisinfected environment [Nde]), 3 days prior to farrowing. Microbiomes of sows and farrowed piglets (n = 27/environment) were profiled at 4 different time points from birth to weaning via 16S rRNA sequencing. The results show that although vaginal, milk, skin, and gut microbiomes in mothers were minimally affected, sanitation of farrowing stalls impacted piglet microbiome colonization. These effects were mainly characterized by lower bacterial diversity in the gut and nasal cavity, specifically in D piglets at birth, and by distinct taxonomic compositions from birth to weaning depending on the farrowing environment. For instance, environmental bacteria greatly influenced microbiome colonization in Nde piglets, which also harbored significantly higher abundances of gut Lactobacillus and nasal Enhydrobacter at several time points through weaning. Different sanitation strategies at birth also resulted in distinct microbiome assembly patterns, with lower microbial exposures in D piglets being associated with limited interactions between bacterial taxa. However, increasing microbial exposures at birth through the lack of disinfection were also associated with lower piglet weight, highlighting the importance of understanding the trade-offs among optimal microbiome development, health, and growth performance in swine production systems. IMPORTANCE We show that levels of disinfection in farrowing facilities can impact early microbial exposures and colonization by pioneer microbes in piglets. Although previous research has shown a similar effect by raising pigs outdoors or by exposing them to soil, these practices are unattainable in most swine production systems in the United States due to biosecurity practices. Thus, our results underscore the importance of evaluating different disinfection practices in swine production to safely reduce pathogenic risks without limiting early microbial exposures. Allowing early exposure to both beneficial and pathogenic microbes may positively impact immune responses, reduce the stressors of weaning, and potentially reduce the need for dietary antimicrobials. However, the benefits of modified early microbial exposures need to be accomplished along with acceptable growth performance. Thus, our results also provide clues for understanding how disinfection practices in farrowing rooms may impact early microbiome development and assembly.

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