Spatio-temporal characteristics of the gastrointestinal resistome in a cow-to-calf model and its environmental dissemination in a dairy production system

Abstract

Microbiome and resistome transmission from mother to child, as well as from animal to environment, has been widely discussed in recent years. Dairy cows mainly provide milk and meat. However, in the dairy production system, the characteristics and transmission trends of resistome assembly and the microbiome in the gastrointestinal tract (GIT) remain unclear. In this study, we sequenced the GIT (rumen fluid and feces) microbiome of dairy cow populations from two provinces in China (136 cows and 36 calves), determined the characteristics of their resistome profiles and the distribution of antibiotics resistance genes (ARGs) across bacteria and further tracked the temporal dynamics of the resistome in offspring during early life using multi-omics technologies (16S ribosomal RNA [rRNA] sequencing, metagenome, and metatranscriptome). We characterized the GIT resistome in cows, distinguished by gut sites and regions. The abundance of ARGs in calves peaked within the first 3 days after birth, with Enterobacteriaceae as the dominant microbial host. As calves aged, resistome composition stabilized, and overall ARG abundance gradually decreased. Both diet and age influenced carbohydrate-active enzymes and ARG profiles. Resistance profiles in ecological niches (meconium, colostrum, soil, and wastewater) were unique, resembling maternal sources. Mobile genetic elements (MGEs), mainly found in soil and wastewater, played an important role in mediating these interactions. Multidrug resistance consistently emerged as the most significant form of resistance at the both the metagenome and metatranscriptome levels. Several antibiotic classes showed higher proportions at the RNA level than at the DNA level, indicating that even low-abundance gene groups can have a considerable influence through high expression. This study broadens our understanding of ARG dissemination in livestock production systems, providing a foundation for developing future preventive and control strategies.