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

Authors: Lyte, Joshua - Josh; KEANE, JAMES - Cork Institute Of Technology; ECKENBERGER, JULIA - University College Cork; ANTHONY, NICHOLAS - University Of Arkansas; SHRESTHA, SANDIP - University Of Arkansas; MARASINI, DAYA - Centers For Disease Control And Prevention (CDC) - United States; DANIELS, KARRIE - Iowa State University; CAPUTI, VALENTINA - University College Cork; Donoghue, Ann - Annie; LYTE, MARK - Iowa State University

Submitted to: Microbiome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/6/2020
Publication Date: 2/2/2021
Citation: Lyte, J.M., Keane, J., Eckenberger, J., Anthony, N., Shrestha, S., Marasini, D., Daniels, K.M., Caputi, V., Donoghue, A.M., Lyte, M. 2021. Japanese quail (Coturnix japonica) as a novel model to study the relationship between the avian microbiome and microbial endocrinology-based host-microbe interactions. Microbiome. https://doi.org/10.1186/s40168-020-00962-2.
DOI: https://doi.org/10.1186/s40168-020-00962-2

Interpretive Summary: The gut is an extension of the outside environment, beginning at the mouth and ending at the anus (in mammals) or cloaca (in birds). Along the gut are several unique areas that have distinct functions of importance to the animal's health. A common feature of all of these areas is that neurohormones, molecules such as serotonin that play many important roles in host health such as regulating mood or in the fight-or-flight response, can be produced throughout the gut. However, the types and amount of neuorhormones produced in different regions of the gut can differ. The bacterial microbiome, which is the collection of bacteria found in the gut, play important roles in affecting animal health. The animal, termed the host, and the microbiome interact in what is called host-microbe interaction and neurohormones serve as a language which allows the animal host and the microbiome to communicate. Stress can affect the host-microbe interaction in the gut through changes in neurohormones. Because neurohormone production is different in different areas of the gut, it is incredibly important to understand how stress affects neurohormone production in different areas of the gut and how this is related to the microbiome, as a greater understanding of this area will lead to new strategies to improve animal health. However, nothing is known how stress affects neurohormone production in the gut of birds and how this is related to the microbiome. As such we sought to investigate how stress affects neurohormone production in different areas of the avian gut, and how this is related to the microbiome. We successfully identified that handling the bird, a simple mild stress, can uniquely affect different regions of the gut and this has distinct relationships to certain bacteria of the microbiome. Our findings will help identify new and future microbiome-based strategies that will help to improve bird health.

Technical Abstract: Background: Microbial endocrinology, which is the study of neuroendocrine interkingdom signaling, provides a causal mechanism-based framework of the importance of host-microbiome bi-directional crosstalk in host health, especially in stress and disease. The importance of the cecal microbiome in avian health is well-recognized yet little is understood regarding the mechanisms underpinning the avian-microbiome relationship. Neuroendocrine plasticity of avian tissues that are focal points of host-microbiome interaction, such as the gastrointestinal tract, has likewise received limited attention. In addition, avian in vivo models that enable the study of the neuroendocrine dynamic between host and microbiome are needed. As such, we utilized Japanese quail that diverge in corticosterone response to stress to examine the relationship between the neuroendocrine biogeography of the avian gastrointestinal tract and the cecal microbiome. Results: Our results demonstrate that birds which contrast in corticosterone response to stress also exhibit divergent region-dependent neuroendocrine plasticity and structural morphologies of the gastrointestinal tract. In addition, neuroendocrine responses to stress which included magnitude of corticosterone response and enteric serotonergic changes associated with profound differences in host cecal microbial community structure. Unique neuroendocrine changes to stress in high stress responsive quail extended to sites outside of the gastrointestinal tract, underscoring the relationship in birds between 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 neuroendocrine changes in the gastrointestinal tract following stress underscores environmental stressors as potential drivers of microbial endocrinology-based mechanisms of avian host-microbiome dialogue. Together, these results demonstrate the regional neuroendocrine plasticity of the avian gastrointestinal tract is 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.