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Review
. 2024 Feb 26;12(3):471.
doi: 10.3390/microorganisms12030471.

The Impact of Early-Life Cecal Microbiota Transplantation on Social Stress and Injurious Behaviors in Egg-Laying Chickens

Affiliations
Review

The Impact of Early-Life Cecal Microbiota Transplantation on Social Stress and Injurious Behaviors in Egg-Laying Chickens

Yuechi Fu et al. Microorganisms. .

Abstract

Injurious behaviors (i.e., aggressive pecking, feather pecking, and cannibalism) in laying hens are a critical issue facing the egg industry due to increased social stress and related health and welfare issues as well as economic losses. In humans, stress-induced dysbiosis increases gut permeability, releasing various neuroactive factors, causing neuroinflammation and related neuropsychiatric disorders via the microbiota-gut-brain axis, and consequently increasing the frequency and intensity of aggression and violent behaviors. Restoration of the imbalanced gut microbial composition has become a novel treatment strategy for mental illnesses, such as depression, anxiety, bipolar disorder, schizophrenia, impulsivity, and compulsivity. A similar function of modulating gut microbial composition following stress challenge may be present in egg-laying chickens. The avian cecum, as a multi-purpose organ, has the greatest bacterial biodiversity (bacterial diversity, richness, and species composition) along the gastrointestinal tract, with vitally important functions in maintaining physiological and behavioral homeostasis, especially during the periods of stress. To identify the effects of the gut microbiome on injurious behaviors in egg-laying chickens, we have designed and tested the effects of transferring cecal contents from two divergently selected inbred chicken lines on social stress and stress-related injurious behaviors in recipient chicks of a commercial layer strain. This article reports the outcomes from a multi-year study on the modification of gut microbiota composition to reduce injurious behaviors in egg-laying chickens. An important discovery of this corpus of experiments is that injurious behaviors in chickens can be reduced or inhibited through modifying the gut microbiota composition and brain serotonergic activities via the gut-brain axis, without donor-recipient genetic effects.

Keywords: aggression; cecal microbiota transplantation; gut microbiota; injurious behavior; laying hen; social stress.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Microbiota profile between two diversely selected chicken lines 63 and 72 (n = 10). (A) Faith’s PD index, values are median ± SEM, a,b indicates significant differences (p ≤ 0.05). (B) Principal coordinate analysis (PCoA) of Bray–Curtis similarity. Each dot represents one bird (n = 10), and PCo1 and PCo2 represent the percentage of variance explained by each coordinate. (C) Cecal microbial composition profiles of the recipient chickens at phylum and genus (relative abundance >2% at phylum, >1% at genus) levels. (D) DESeq2 analysis of differentially abundant ASVs between line 63 and line 72. Estimations of log2 fold change values for each ASV were computed and each point represents an ASV that was significantly different (p ≤ 0.05) [106].
Figure 2
Figure 2
Timeline of the experimental design of trial 2 and trial 3 and the proposed mechanisms underlying the transplant effects on health and behavior of recipient chickens.
Figure 3
Figure 3
Effects of cecal microbiota transplantation on (A) body weight of recipient roosters; ileal morphology of recipient roosters in week 5 (B) and week 16 (C). Ileal villus height (VH), crypt depth (CD), and VH/CD ratio. Values are least-squares means ± SEM, n = 7. a,b indicate significant differences (p ≤ 0.05). Abbreviations: 63-CMT, chickens with cecal bacterial solution of donor line 63; 72-CMT, chickens with cecal bacterial solution of donor line 72; CTRL, control; CD, crypt depth; VH, villus height [106].
Figure 4
Figure 4
Effects of cecal microbiota transplantation on ileal serotonergic activities of recipient roosters. Serotonergic activity in week 5 (A,B) and week 16 (C,D). Values are least-squares means ± SEM, n = 7. a,b indicate significant differences (P ≤ 0.05), A,B show trend differences (0.05 < P ≤ 0.10). Abbreviations: 5-HIAA, 5-hydroxuindoleacetic acid; 5-HT, serotonin; 63-CMT, chickens with cecal bacterial solution of donor line 63; 72-CMT, chickens with cecal bacterial solution of donor line 72; CTRL, control [106].
Figure 5
Figure 5
Frequency of aggressive pecking of recipient chickens in week 5 and week 16. (A) Home-cage behavior. (B) Paired test. Values are means ± SEM, n = 7. * indicates significant differences (p ≤ 0.05), and # shows trend differences (0.05 < p ≤ 0.1). 63-CMT, received cecal content solution from 63 donors; 72-CMT, received cecal content solution from 72 donors; CTRL, received saline, control [123].
Figure 6
Figure 6
Effects of cecal microbiota transplantation on cecal microbial profiles of recipient chickens in week 5 and week 16 (n = 7). (A) Faith’s PD index, values are median ± SEM, * indicates significant differences (p ≤ 0.05), and # shows trend differences (0.05 < p ≤ 0.1). (B) Principal coordinate analysis (PCoA) of Unweighted UniFrac of recipient chickens in week 5 and week 16. Each dot represents one bird (n = 7), and PCo1 and PCo2 represent the percentage of variance explained by each coordinate. (C) DESeq2 analysis of differentially abundant ASVs between 63-CMT group and 72-CMT group in week 5 and week 16. Estimations of log2 fold change values for each ASV were computed and each point represents an ASV that was significantly different (p ≤ 0.05). 63-CMT, received cecal content solution from 63 donors; 72-CMT, received cecal content solution from 72 donors; CTRL, received saline, control [123].

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