Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome

Authors: Lyte, Joshua - Josh; ECKENBERGER, JULIA - University College Cork; KEANE, JAMES - University College Cork; Robinson, Kelsy; Bacon, Tyler; FACCHETTI, ASSUMPCAO - University Of Arkansas; Donoghue, Ann - Annie; LIYANAGE, ROHANA - University Of Arkansas; DANIELS, KARRIE - Iowa State University; Caputi, Valentina; LYTE, MARK - Iowa State University

Submitted to: Poultry Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/15/2023
Publication Date: 3/1/2024
Citation: Lyte, J.M., Eckenberger, J., Keane, J., Robinson, K., Bacon, T.F., Facchetti, A., Donoghue, A.M., Liyanage, R., Daniels, K.M., Caputi, V., Lyte, M. 2024. Cold stress initiates catecholaminergic and serotonergic responses in the chicken gut that are associated with functional shifts in the microbiome. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 103(3). Article 103393. https://doi.org/10.1016/j.psj.2023.103393.
DOI: https://doi.org/10.1016/j.psj.2023.103393

Interpretive Summary: The temperature of the environment in which chickens are raised is an important factor for poultry production. Following hatch, chicks require a warm environment. Temperatures that do not achieve this level of warmth can negatively affect growth performance as well as cause stress leading to increased susceptibility to disease and foodborne pathogen carriage. Hence, cold temperatures in the production environment are form of stress that is responsible for major economic loss to the poultry industry and a potential driver of foodborne pathogen carriage in pre-harvest chickens. As foodborne pathogen carriage happens in the chicken gut, it is important to understand how cold stress may affect the chicken gut to make it more susceptible to bacterial colonization. One route by which stress can increase bacterial colonization is through the fight-or-flight response which includes the production of stress-related neurochemicals. However, it is unknown how cold stress increases foodborne pathogen carriage, and if intestinal neurochemical concentrations are increased following this form of stress. We sought to determine whether cold stress during the first week post-hatch increases stress-related neurochemical concentrations in the chick gut, and if these neurochemical concentrations are permanently altered throughout the production life of the chicken. As the gut also contains normal populations of bacteria, called the microbiota, we also sought to determine the impact of cold stress on the population and function of the microbiota. Our results identified that cold stress initiates distinct neurochemical responses in the chick gut and significantly changes the microbiome. Importantly, the amount of neurochemicals as well as shifts in the microbiome remain altered for weeks following the stress. These findings establish the gut fight-or-flight neurochemical response as a potential platform to prevent stress-driven increases in foodborne pathogen carriage in pre-harvest poultry.

Technical Abstract: Despite being well-documented in mammals, the effect of environmental stress on enteric neurophysiology and concomitant impact on host-microbiome interactions remains poorly understood in birds. As early life stressors may imprint long-term adaptive changes in the host, the present study sought to determine whether cold stress, a prominent form of early life stress in chickens, elicits enteric stress-related neurochemical responses that coincide with compositional and functional changes in the microbiome that persist into the later life of the bird. Chicks were, or were not, subjected to cold stress during the first week post-hatch and then remained at normotemperature for the remainder of the study. 16S rRNA and shallow shotgun metagenomic analyses demonstrated taxonomic and functional separation between the cecal microbiomes of control and cold stressed chickens. Changes in the concentration of monoamine neurochemicals were found in both cecal tissue and luminal content of cold stressed chickens. Significant associations were identified between cecal neurochemical concentrations and microbial taxa, suggesting host enteric neurochemical responses to environmental stress may shape the cecal microbiome. As many neurochemicals serve as interkingdom signaling molecules, the relationships identified here could be exploited to control the impact of stress on avian enteric host-microbe interactions.