Integrated multi-omics reveals the roles of cecal microbiota and its derived bacterial consortium in promoting chicken growth

Abstract

ABSTRACT Growing evidence has shown a close connection between gut microbiota and chicken growth performance; however, the crosstalk between microbes and chicken host remains elusive. Here, we integrated multi-omics approaches, fecal microbiota transplantation, and body weight-associated bacterial consortium to investigate the host-microbiota interactions in different body weight chickens. Microbial profiling analysis showed that uncultured Barnesiellaceae , Lactobacillus , Bacillus , Ruminococcaceae UCG-004 , and Ruminococcaceae UCG-014 were highly enriched in the high body weight (HBW) chickens. The combination of Lactobacillus and Bacillus had 95.1% accuracy in discriminating HBW from low body weight chickens. Lipids and lipid-like molecules were found to be more abundant in the HBW chickens, and the differentially expressed cecal genes were enriched in the peroxisome proliferator-activated receptor (PPAR) signaling pathway and calcium signaling pathway. Correlations among the weight-associated genera, gut content metabolites, and gut gene expression were established, and fecal microbiota transplantation from HBW microbiota to newly born chicks increased the chicken antioxidant status, gut sugar transport, and immunity. A total of 67 strains belonging to Lactobacillus and Bacillus were isolated from the HBW chickens by the targeted culturomics method. Among six pairwise combinations of four selected strains, the consortium consisting of Limosilactobacillus reuteri CML393 and Bacillus velezensis CML396 significantly improved the chicken growth performance and gut health and influenced the cecal microbiota, metabolites, and gene expression. Further in vitro and in silico analyses indicated that L. reuteri CML393 and B. velezensis CML396 were less competitive but more cooperative than other pairwise combinations tested. IMPORTANCE The improvement of chicken growth performance is one of the major concerns for the poultry industry. Gut microbes are increasingly evidenced to be associated with chicken physiology and metabolism, thereby influencing chicken growth and development. Here, through integrated multi-omics analyses, we showed that chickens from the same line differing in their body weight were very different in their gut microbiota structure and host-microbiota crosstalk; microbes in high body weight (HBW) chickens contributed to chicken growth by regulating the gut function and homeostasis. We also verified that a specific bacterial consortium consisting of isolates from the HBW chickens has the potential to be used as chicken growth promoters. These findings provide new insights into the potential links between gut microbiota and chicken phenotypes, shedding light on future manipulation of chicken gut microbiota to improve chicken growth performance.