Connecting gut microbiomes and short chain fatty acids with the serotonergic system and behavior in Gallus gallus and other avian species

Abstract

The chicken gastrointestinal tract has a diverse microbial community. There is increasing evidence for how this gut microbiome affects specific molecular pathways and the overall physiology, nervous system and behavior of the chicken host organism due to a growing number of studies investigating conditions such as host diet, antibiotics, probiotics, and germ-free and germ-reduced models. Systems-level investigations have revealed a network of microbiome-related interactions between the gut and state of health and behavior in chickens and other animals. While some microbial symbionts are crucial for maintaining stability and normal host physiology, there can also be dysbiosis, disruptions to nutrient flow, and other outcomes of dysregulation and disease. Likewise, alteration of the gut microbiome is found for chickens exhibiting differences in feather pecking (FP) behavior and this alteration is suspected to be responsible for behavioral change. In chickens and other organisms, serotonin is a chief neuromodulator that links gut microbes to the host brain as microbes modulate the serotonin secreted by the host’s own intestinal enterochromaffin cells which can stimulate the central nervous system via the vagus nerve. A substantial part of the serotonergic network is conserved across birds and mammals. Broader investigations of multiple species and subsequent cross-comparisons may help to explore general functionality of this ancient system and its increasingly apparent central role in the gut-brain axis of vertebrates. Dysfunctional behavioral phenotypes from the serotonergic system moreover occur in both birds and mammals with, for example, FP in chickens and depression in humans. Recent studies of the intestine as a major site of serotonin synthesis have been identifying routes by which gut microbial metabolites regulate the chicken serotonergic system. This review in particular highlights the influence of gut microbial metabolite short chain fatty acids (SCFAs) on the serotonergic system. The role of SCFAs in physiological and brain disorders may be considerable because of their ability to cross intestinal as well as the blood-brain barriers, leading to influences on the serotonergic system via binding to receptors and epigenetic modulations. Examinations of these mechanisms may translate into a more general understanding of serotonergic system development within chickens and other avians.

Use of Monoglycerides and Diglycerides to Mitigate Poultry Production Losses: A Review

“…Officially, FFAR2 appears to be the only reported FFAR gene in the chicken genome, while many mammal genomes have four identified FFAR genes [ 71 , 72 ]. However, some studies have evaluated the expression of other putative FFAR genes in chickens and found them to be associated with oral and intestinal nutrient sensing; serotonin expression and behavior; PPAR-related gluconeogenesis; and immune cell regulation [ 73 , 74 , 75 , 76 ]. In mammals, the different FFAR genes have an affinity for FA of different lengths.…”

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

“…Line 7 2 chickens have lower levels of brain serotonin (5-HT) than line 6 3 chickens. Serotonin dysregulation has been implicated in a range of neuropsychiatric disorders in humans and various animals including chickens [ 118 , 119 ]. Lower levels of 5-HT have also been found in the brain of violent offenders [ 120 , 121 , 122 ].…”

“…Accumulating studies from various animal models in gut microbiota investigations, such as GF (complete absence of microbial exposure) animals, SPF (specific pathogen-free) animals, antibiotic-treated (broad-spectrum antibiotic cocktails) animals, and animals exposed to pathogenic bacterial infections, suggest that the gut microbiota plays an important role in the regulation of anxiety, mood, and cognition, indicating the possibility of using probiotics to modify the gut microbiota to control impulsive and compulsive behaviors in patients with neuropsychiatric disorders [ 158 , 159 , 160 , 161 ]. Like mammals, the gut microbiome plays a critical role in poultry health and welfare [ 119 , 162 , 163 ]. Laying hens showing high or low FP have different gut microbial populations [ 27 , 94 , 95 , 164 ] and metabolite profiles [ 96 , 97 ].…”

Gut microbiome-brain crosstalk in the early life of chicken reveals the circadian regulation of key metabolic and immune signaling processes

“…These studies re ect the key interactions between neural factors, the gut microbiome, and GALT physiology. In avian species, there is emerging evidence of the gut-brain crosstalk [27][28][29] suggesting similar mechanisms as in mammalian models.…”