Serotonin modulates Campylobacter jejuni physiology and in vitro interaction with the gut epithelium

Authors: Lyte, Joshua - Josh; SHRESTHA, SANDIP - University Of Arkansas; WAGLE, BASANTA - University Of Arkansas; LIYANGE, ROHANA - University Of Arkansas; MARTINEZ, DIEGO - University Of Arkansas; Donoghue, Ann - Annie; DANELS, KARRIE - Iowa State University; LYTE, MARK - Iowa State University

Submitted to: Poultry Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/15/2020
Publication Date: 3/3/2021
Citation: Lyte, J.M., Shrestha, S., Wagle, B.R., Liyange, R., Martinez, D.A., Donoghue, A.M., Danels, K.M., Lyte, M. 2021. Serotonin modulates Campylobacter jejuni physiology and in vitro interaction with the gut epithelium. Poultry Science. 100(3). Article 100944. https://doi.org/10.1016/j.psj.2020.12.041.
DOI: https://doi.org/10.1016/j.psj.2020.12.041

Interpretive Summary: Campylobacter jejuni is a bacterial species often found in the intestinal tract of chickens. Because chickens are a food source for people, C. jejuni contamination of chicken meat and products can lead to C. jejuni infection in people. As C. jejuni is a major cause of foodborne illness in people, strategies are needed to reduce the presence of C. jejuni in the chicken intestinal tract. In the chicken intestinal tract, neurochemicals (such as serotonin) are produced. Neurochemicals serve as a language between host (e.g. the chicken) and bacteria, and certain neurochemicals are known to affect bacterial growth or change their interaction with the host. Serotonin is a neurochemical that is produced in the gut and is known to affect bacteria, however it is unknown if it affects C. jejuni. We therefore investigated if serotonin can cause changes in C. jejuni physiology and interaction with the host. We identified that serotonin does affect C. jejuni physiology and colonization of a cell model of the gut epithelium. As serotonin production in the gut can change in response to different conditions, such as stress, we have identified a neurochemical on which strategies can be developed to reduce C. jejuni presence in the chicken gut, thereby potentially leading to safer poultry products.

Technical Abstract: Microbial endocrinology, which is the study of neurochemical-based host-microbe interaction, has demonstrated that neurochemicals affect bacterial pathogenicity. A variety of neurochemicals, including norepinephrine, were shown to enhance intestinal epithelial colonization by Campylobacter jejuni. Yet, little is known whether serotonin, an abundant neurochemical produced in the gut, affects the physiology of C. jejuni and its interaction with the host gut epithelium. Considering the avian gut produces serotonin and serves as a major reservoir of C. jejuni, we sought to investigate whether serotonin can affect C. jejuni physiology and gut epithelial colonization in vitro. We first determined the biogeographical distribution of serotonin concentrations in the serosa, mucosa, as well as the luminal contents of the broiler chicken ileum, cecum, and colon. Serotonin concentrations were greater (p<0.05) in the mucosa and serosa compared to the luminal content in each gut region examined. Among the ileum, colon, and cecum, the colon was found to contain the greatest (p<0.05) concentrations of serotonin. We then investigated whether serotonin may effect changes in C. jejuni growth and motility in vitro. The C. jejuni used in this study was previously isolated from the broiler chicken ceca. Serotonin at each concentration tested did not elicit changes in growth (p>0.05) or motility (p>0.05) of C. jejuni. Next, we utilized liquid chromatography tandem mass spectrometry to investigate whether serotonin affected the proteome of C. jejuni. Serotonin caused (p<0.05) the downregulation of a protein (CJJ81176_1037) previously identified to be essential in C. jejuni colonization. Based on our findings, we evaluated whether serotonin would cause a functional change in C. jejuni adhesion and invasion of the HT29MTX-E12 colonic epithelial cell line. Serotonin was found to cause a reduction in adhesion (p<0.05) but not invasion (p>0.05). Together, we have identified a potential role for serotonin in modulating C. jejuni colonization in the gut in vitro. Further studies are required to understand the practical implications of these findings for the control of C. jejuni enteric colonization in vivo.