Oxygen deprivation influences the survival of listeria monocytogenes in gerbils

Authors: HARRIS, JILLIAN - Mississippi State University; PAUL, OINDRILA - University Of Southern Mississippi; PARK, SI - University Of Arkansas; WHITE, SALLY - University Of Southern Mississippi; BUDACHETRI, KHEM - University Of Southern Mississippi; MCCLUNG, DANIEL - Mississippi State University; WILSON, JESSICA - University Of Central Florida; OLIVIER, ALICIA - Mississippi State University; THORNTON, JUSTIN - Mississippi State University; Broadway, Paul; RICKE, STEVEN - University Of Arkansas; DONALSON, JANET - University Of Southern Mississippi

Submitted to: Translational Animal Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2018
Publication Date: 1/1/2019
Citation: Harris, J., Paul, O., Park, S.H., White, S.J., Budachetri, K., Mcclung, D.M., Wilson, J.G., Olivier, A.K., Thornton, J.A., Broadway, P.R., Ricke, S.C., Donalson, J.R. 2019. Oxygen deprivation influences the survival of listeria monocytogenes in gerbils. Translational Animal Science. 3:304-314. https://doi.org/10.1093/tas/txy110.
DOI: https://doi.org/10.1093/tas/txy110

Interpretive Summary: Listeria is a foodborne pathogen that can cause a disease known as listeriosis, and this bacteria my lead to abortions in pregnant women. The availability of oxygen in the gastrointestinal tract may influence the growth and survivability of the pathogen. This phenomenon may also be linked to other inflammatory infections in the intestine. Therefore, the objective of this study was to evaluate what changes occurred in gerbils following a Listeria infection in which Listeria were cultured with various concentrations of oxygen. A total of 28 gerbils were utilized for this study. Gerbils were divided into groups of 7 and orally administered Listeria grown in low or high aerobic conditions or low or high anaerobic conditions. At the end of the 5 day study, there were no differences in gerbil weight. Gerbils inoculated with a low anaerobic dose or high aerobic dose had greater fecal shedding of listera after 5 days of infection. After 5 days, the gerbils were humanely euthanized, and tissues were collected for Listeria isolation. However, minimal differences were observed in Listeria concentrations amongst the tissues from each treatment. Sections of tissues were also examined microscopically, but similar to bacterial concentrations, few differences were noted amongst the treatments. While few overall differences existed between the treatments, gerbils given high anaerobic Listeria exhibited greater signs of illness and some experienced mortality prior to the conclusion of the study. Additionally, the different treatments caused a slight shift in the overall microbial populations of the small intestine. Further research is needed to fully understand the changes that occur during Listeria infections under different anaerobic conditions.

Technical Abstract: Listeria monocytogenes is a facultative anaerobic foodborne pathogen capable of surviving harsh environments. Recent work has indicated that anaerobic conditions increase the resistance capability of certain strains to environmental stressors. This study’s goal was to determine if oxygen exposure prior to infection increases the ability to survive in vivo. Gerbils were inoculated with one of 5 doses of the strain F2365 by oral gavage: phosphate buffered saline (PBS; control), 5x106 CFU aerobic culture (low aerobic), 5x108 aerobic culture (high aerobic), 5x106 anaerobic culture (low anaerobic), or 5x108 anaerobic culture (high anaerobic) dose of F2365. Gerbils inoculated with a high aerobic or anaerobic dose exhibited significant weight loss. Gerbils administered either the low or high anaerobic dose had at least 3 Log10 of L. monocytogenes present in fecal samples, which contrasted with gerbils that received the low aerobic dose. Animals that received the high anaerobic dose had a significant increase in bacterial loads within the liver. Histologic examination of the L. monocytogenes positive livers exhibited locally extensive areas of hepatocellular necrosis, though the extent of this damage differed between treatment groups. Microbial community analysis of the cecum from gerbils infected with L. monocytogenes indicated that the abundance of Bacteroidales and Clostridiales increased and there was a decrease in the abundance of Spirochaetales. This study indicates that anaerobic conditions alter the localization pattern of L. monocytogenes within the gastrointestinal tract. These findings could relate to how different populations are more susceptible to listeriosis, as oxygen availability may differ within the gastrointestinal tract.