Japanese quail (Coturnix japonica) as a novel model to study the relationship between the avian microbiome and microbial endocrinology-based host-microbe interactions

Abstract

Background Microbial endocrinology, which is the study of neuroendocrine-based interkingdom signaling, provides a causal mechanistic framework for understanding the bi-directional crosstalk between the host and microbiome, especially as regards the effect of stress on health and disease. The importance of the cecal microbiome in avian health is well-recognized, yet little is understood regarding the mechanisms underpinning the avian host-microbiome relationship. Neuroendocrine plasticity of avian tissues that are focal points of host-microbiome interaction, such as the gut and lung, has likewise received limited attention. Avian in vivo models that enable the study of the neuroendocrine dynamic between host and microbiome are needed. As such, we utilized Japanese quail (Coturnix japonica) that diverge in corticosterone response to stress to examine the relationship between stress-related neurochemical concentrations at sites of host-microbe interaction, such as the gut, and the cecal microbiome. Results Our results demonstrate that birds which contrast in corticosterone response to stress show profound separation in cecal microbial community structure as well as exhibit differences in tissue neurochemical concentrations and structural morphologies of the gut. Changes in neurochemicals known to be affected by the microbiome were also identified in tissues outside of the gut, suggesting a potential relationship in birds between the cecal microbiome and overall avian physiology. Conclusions The present study provides the first evidence that the structure of the avian cecal microbial community is shaped by selection pressure on the bird for neuroendocrine response to stress. Identification of unique region-dependent neurochemical changes in the intestinal tract following stress highlights environmental stressors as potential drivers of microbial endocrinology-based mechanisms of avian host-microbiome dialogue. Together, these results demonstrate that tissue neurochemical concentrations in the avian gut may be related to the cecal microbiome and reveal the Japanese quail as a novel avian model in which to further examine the mechanisms underpinning these relationships.

Microbiota and stress: a loop that impacts memory

“…CRHR1 is an essential regulator of the HPA axis; its hippocampal expression has also been shown to be reduced by maternal separation in mice 58 and CRHR1 -deficient mice are unable to mount a corticosterone response to stress 59 . Moreover, this reduction in plasma corticosterone levels under basal conditions has previously been described in European starling 60, 61 and in this line of quail subjected to a chronic stress procedure 40 , whereas more acute stress increases corticosterone levels in this species 38 . We found reduced PCNA expression in the hypothalamus of the STRESS-T group, which suggests decreased cell proliferation.…”

“…Japanese quails were used because we have already shown that their anxiety-like behavior and memory properties are impacted by a chronic stress procedure (unpredictable repeated negative stimuli for 21 days) 32,33 and gut microbiota manipulations (germ-free model, microbiota transfer and probiotic supplementation) [34][35][36][37] . Moreover, Japanese quail have recently been suggested as a relevant model to study the involvement of gut microbiota in stress processes 38 . Here, the approach of cecal microbiota transfer (CMT) was used involving the transfer of microbiota from a chronically-stressed individual to germ-free naïve quails to investigate whether the CMT induced any negative consequences on quails' spatial and cue-based memory abilities as previously demonstrated in the stressed donors 32 .…”

Gut Microbiota Linked with Reduced Fear of Humans in Red Junglefowl Has Implications for Early Domestication

“…In contrast to our observed association of Lactobacillus with fear behavior, we observed that Clostridiales were enriched in the low fear fowl and several unknown Clostridiales species have been associated with reduced stress in Japanese quail. [ 40 ] This observation is interesting in light of previous findings associating these taxa with impaired fear memory in obese mice, including members of the orders Lachnospiraceae and Ruminococcaceae . [ 41 ] Clostridiales are also known to promote host serotonin biosynthesis [ 42 ] and higher blood serotonin has been observed in the low fear red junglefowl males.…”

Role of diet-microbiota interactions in precision nutrition of the chicken: facts, gaps, and new concepts

“…As described previously, the avian gut microbiota along with their genes and gene products (the microbiome), perform several functions that heavily impact host physiology. Not only does the gut microbiome play a critical role in modulating host immune defense ( Kogut et al, 2017 ; Broom and Kogut, 2018 ), brain function ( Villageliu and Lyte, 2018 ; Lyte et al, 2021 ), host metabolism regulation ( Stanley et al, 2014 ; Lyte et al, 2021 ; Zhang et al, 2021 ), but also other physiological processes and characteristics thought to depend solely on the genetic program of the bird; gut-liver axis ( Bao et al, 2021 ), gut-bone axis ( Wideman et al., 2012 ; Tomaszewska et al, 2015 ; Airubaye et al, 2020 ), and gut-muscle axis ( Zhang et al, 2021 ). A greater understanding of the key signaling pathways of the cross-species homeostatic regulation between the gut microbiota and its host implicated in these axes are a prerequisite for optimizing therapeutic dietary strategies to manipulate the gut microbiota.…”