Antimicrobial Growth Promoters Altered the Function but Not the Structure of Enteric Bacterial Communities in Broiler Chicks ± Microbiota Transplantation

SIMPLE SUMMARY: The use of antimicrobial growth promoters (AGPs) is no longer allowed in livestock production in many jurisdictions globally due to the potential emergence of antimicrobial resistance in zoonotic bacteria. Understanding the mode of action of AGPs may aid in the development of effective alternatives, and we examined the impact of the conventional antibiotic AGP, virginiamycin, and an AGP alternative, ceragenin (CSA-44), on the structure and function of the intestinal microbiota in young broiler chickens. Additionally, the temporal establishment of intestinal bacterial communities ± administration of virginiamycin and CSA-44 was evaluated by transplanting microbiota from healthy adult donor chickens into 1-day-old chicks. Microbiota transplantation showed an early establishment of a stable and diverse bacterial community. Neither virginiamycin nor CSA-44 impacted bird growth or the structure of bacterial communities regardless of microbiota transplantation. However, the complexity of the intestinal bacterial community in birds administered virginiamycin and CSA-44 affected the quantity and type of metabolites produced. Study findings demonstrate that the evaluation of effective AGP alternatives must comprehensively address their effects on the host–microbiota interaction, including impacts on the function of the intestinal microbiota. ABSTRACT: Non-antibiotic alternatives to antimicrobial growth promoters (AGPs) are required, and understanding the mode of action of AGPs may facilitate the development of effective alternatives. The temporal impact of the conventional antibiotic AGP, virginiamycin, and an AGP alternative, ceragenin (CSA-44), on the structure and function of the broiler chicken cecal microbiota was determined using next-generation sequencing and (1)H-nuclear magnetic resonance spectroscopy (NMR)-based metabolomics. To elucidate the impact of enteric bacterial diversity, oral transplantation (±) of cecal digesta into 1-day-old chicks was conducted. Microbiota transplantation resulted in the establishment of a highly diverse cecal microbiota in recipient chicks that did not change between day 10 and day 15 post-hatch. Neither virginiamycin nor CSA-44 influenced feed consumption, weight gain, or feed conversion ratio, and did not affect the structure of the cecal microbiota in chicks possessing a low or high diversity enteric microbiota. However, metabolomic analysis of the cecal contents showed that the metabolome of cecal digesta was affected in birds administered virginiamycin and CSA-44 as a function of bacterial community diversity. As revealed by metabolomics, glycolysis-related metabolites and amino acid synthesis pathways were impacted by virginiamycin and CSA-44. Thus, the administration of AGPs did not influence bacterial community structure but did alter the function of enteric bacterial communities. Hence, alterations to the functioning of the enteric microbiota in chickens may be the mechanism by which AGPs impart beneficial health benefits, and this possibility should be examined in future research.