Cecal microbiota transplantation: Unique influence of cecal microbiota from divergently selected inbred donor lines on cecal microbial profile, serotonergic activity, and aggressive behavior of recipient chickens

Authors: FU, YUECHI - Purdue University; HU, JIAYING - Purdue University; ERASMUS, MARISA - Purdue University; Zhang, Huanmin; JOHNSON, TIMOTHY - Purdue University; Cheng, Heng-Wei

Submitted to: Journal of Animal Science and Biotechnology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/9/2023
Publication Date: 5/2/2023
Citation: Fu, Y., Hu, J., Erasmus, M.A., Zhang, H., Johnson, T.A., Cheng, H. 2023. Cecal microbiota transplantation: Unique influence of cecal microbiota from divergently selected inbred donor lines on cecal microbial profile, serotonergic activity, and aggressive behavior of recipient chickens. Journal of Animal Science and Biotechnology. 14(1)Article 66. https://doi.org/10.1186/s40104-023-00866-9.
DOI: https://doi.org/10.1186/s40104-023-00866-9

Interpretive Summary: Gut bacteria play an important role in the bidirectional interactions between the gut and brain. Modification of gut bacterial composition has been a novel therapy for treating patients with neuropsychiatric disorders. Injurious behavior is one of the top health and welfare issues in laying hens. Beak trimming is routinely used management practice to prevent or reduce injurious pecking in laying hens, but it has been long criticized to cause welfare issues itself, including pain, stress, and beak malfunction. The goal of this project is to examine if injurious behavior in laying hens can be prevented or reduced by modification of gut bacteria. The current objective was to examine if cecal bacteria transplantation reduces aggression in chickens. To reach the aim, the divergently selected inbred chicken lines 63 (gentle birds) and 72 (aggressive birds) were used as donors and a commercial chicken line was used as recipients. The results indicate that that early postnatal cecal bacterial transplantation has the potential to reduce aggressive behaviors and improve health in chickens through regulating the gut-immune-brain axis. The findings may provide insights for egg producers and animal scientists to develop novel management strategies for improving poultry health and welfare.

Technical Abstract: Accumulating evidence from human trials and rodent studies has indicated that modulation of gut microbiota affects host physiological homeostasis and behavioral characteristics. Similarly, alterations in gut microbiota could be a feasible strategy for reducing aggressive behavior and improving health in chickens. The study was conducted to determine the effects of early-life cecal microbiota transplantation (CMT) on cecal microbial composition, brain serotonergic activity, and aggressive behavior of recipient roosters. In the study, chicken lines 63 and 72 with nonaggressive and aggressive behavior, respectively, were used as donors and a commercial strain Dekalb XL was used as recipient birds for CMT. Eight-four one-day-old male chicks were randomly assigned to 1 of 3 treatments with 7 cages per treatment and 4 birds per cage (n=7): saline (control, CTRL), cecal solution of line 63 (63-CMT), and cecal solution of line 72 (72-CMT). Transplantation was conducted via oral gavage once daily from day 1 to 10, and then boosted once weekly from week 3 to 5. At week 5 and 16, home-cage behavior was recorded, and birds with similar body weights were assigned to paired aggression tests between the treatments. Samples of blood, brain, and cecal contents were collected from the post-tested birds to detect CMT-induced biological and microbiota changes. The results indicate that 63-CMT birds displayed less aggressive behavior with a higher hypothalamic serotonergic activity at week 5. Correspondingly, one Ruminococcaceae UCG-005 amplicon sequence variant (ASV) and two Lachnospiraceae ASVs were positively correlated with levels of brain serotonin and tryptophan, respectively. 72-CMT birds had lower levels of brain norepinephrine and dopamine at week 5 with higher levels of plasma serotonin and tryptophan at week 16. ASVs belonging to Mollicutes RF39 and GCA-900066225 were negatively correlated with brain 5-hydroxuindoleacetic acid (5-HIAA) at week 5, and one Bacteroides ASV was negatively correlated with plasma serotonin at week 16 in 72-CMT birds. In conclusion, CMT at an early age could regulate aggressive behavior via modulating the cecal microbial composition, along with central serotonergic and adrenergic systems in recipient birds. The CMT could be a novel strategy for reducing aggressive behavior through regulating signaling along the microbiota-gut-brain axis.