A neurochemical biogeography of the broiler chicken intestinal tract

Authors: Lyte, Joshua - Josh; MARTINEZ, DIEGO - University Of Arkansas; Robinson, Kelsy; Donoghue, Ann - Annie; DANIELS, KARRIE - Iowa State University; LYTE, MARK - Iowa State University

Submitted to: Poultry Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/10/2021
Publication Date: 3/1/2022
Citation: Lyte, J.M., Martinez, D.A., Robinson, K., Donoghue, A.M., Daniels, K.M., Lyte, M. 2022. A neurochemical biogeography of the broiler chicken intestinal tract. Poultry Science. 101(30). Article 101671. https://doi.org/10.1016/j.psj.2021.101671.
DOI: https://doi.org/10.1016/j.psj.2021.101671

Interpretive Summary: Microbial endocrinology is a field of research that is focused on how the host (i.e. the animal) communicates at a molecular level with microorganisms (e.g. bacteria) through neurochemicals. Some bacteria, such as Campylobacter jejuni or Salmonella, can be found in the chicken gut and are known foodborne pathogens in people. In addition, many of these foodborne pathogen-relevant bacteria respond to neurochemicals, therefore emphasizing the need to understand how in the chicken gut do neurochemicals influence host-microbe interactions. While it has been known for decades that neurochemicals are produced in the chicken intestinal tract, little is known how different regions of the gut may differ in what neurochemical are present, or at what concentrations they are found. Along the length of the gut are many different physiological regions, and specific bacteria often have special strategies to infect or colonize only certain areas of the gut. It is therefore critically important to identify concentrations of neurochemicals in each intestinal region in order to better understand what neurochemical host-microbe interactions may be occurring in each region of the gut. This would allow the design of tailored region-specific neuorchemical-based strategies to eliminate foodborne pathogen bacteria in the chicken gut, and improve consumer food safety of poultry products. We therefore investigated the neurochemical concentrations of each major intestinal region of the chicken intestinal tract. We identified that what neurochemicals are present and at what concentrations are often unique to different areas of the gut. This information provides an important foundation for poultry researchers in the design of neurochemical-based strategies to improve food safety of poultry products through the elimination of foodborne bacteria in the chicken gut.

Technical Abstract: The study of neurochemical-based interkingdom signaling and its impact on host-microbe interaction is called microbial endocrinology. Neurochemicals play a recognized role in determining bacterial colonization and interaction with the gut epithelium. While much attention has been devoted to the determination of neurochemical concentrations in the mammalian gut to better understand tissue and region-specific microbial endocrinology-based mechanisms of host-microbe interaction, little is known regarding the biogeography of neurochemicals in the avian gut. Greater resolution of avian gut neurochemical concentrations is needed, especially as recent microbial endocrinology-based investigations into bacterial foodborne pathogen colonization of the chicken gut have demonstrated neurochemicals to affect Campylobacter jejuni and Salmonella spp. in vivo and in vitro. The aim of the present study was to determine the concentrations of stress-related neurochemicals in the tissue and luminal content of the duodenum, jejunum, ileum, cecum, and colon of the broiler intestinal tract, and to investigate if this biogeography changes with age of the bird. While all neurochemicals measured were detected in the intestinal tract, many displayed differences in regional concentrations. Whereas the catecholamine norepinephrine was detected in each region of the intestinal tract, epinephrine was present only in the cecum and colon. Likewise, dopamine, and its metabolite 3,4-dihydroxyphenylacetic acid were found in the greatest quantities in the cecum and colon. Serotonin and histamine were identified in each gut region. Region-specific age-related changes were observed (P<0.05) for serotonin, its metabolite 5-hydroxyindole acetic acid as well as for histamine. Several neurochemicals, including norepinephrine, were found in the contents of each gut region. Epinephrine was not detected in the gut content of any region. Salsolinol, a microbial-produced neuroactive compound was detected in the gut content but not in tissue. Together, our data establish a neurochemical biogeography of the broiler chicken intestinal tract. By providing researchers with a region-by-region map of in vivo gut neurochemical concentrations of a modern broiler chicken breed, this neurochemical map is expected to inform future investigations that seek to utilize avian enteric neurochemistry.