Activation of aryl hydrocarbon receptor by dioxin directly shifts gut microbiota in zebrafish

Yumiao SUN, Lizhu TANG, Yang LIU, Chenyan HU, Bingsheng ZHOU, Paul K.S. LAM, Chung Wah James LAM, Lianguo CHEN

Research output: Contribution to journalArticle

Abstract

Gut microbiota is of critical importance to host health. Aryl hydrocarbon receptor (AhR) is found to be closely involved in the regulation of gut microbial dynamics. However, it is still not clear how AhR signaling shapes the gut microbiota. In the present study, adult zebrafish were acutely exposed to an AhR antagonist (CH223191), an AhR agonist (polychlorinated biphenyl 126; PCB126) or their combination for 7 d. Overall intestinal health and gut microbial community were temporally monitored ( 1 d, 3 d and 7 d) and inter-compared among different groups. The results showed that single exposure to PCB126 significantly disrupted the overall health of intestines (i.e., neural signaling, inflammation, epithelial barrier integrity, oxidative stress). However, CH223191 failed to inhibit but enhanced the physiological toxicities of PCB126, implying the involvement of extra mechanisms rather than AhR in the regulation of intestinal physiological activities. Dysbiosis of gut microbiota was also caused by PCB126 over time as a function of sex. It is intriguing that CH223191 successfully abolished the holistic effects of dioxin on gut microbiota, which inferred that growth of gut microbes was directly controlled by AhR activation without the involvement of host feedback modulation. When coming to detailed alterations at certain taxon, both antagonistic and synergistic interactions existed between CH223191 and dioxin, depending on fish sex, exposure duration and bacterial species. Correlation analysis found that gut inflammation was positively associated with pathogenic Legionella bacteria, but was negatively associated with epithelial barrier integrity, suggesting that integral intestinal epithelial barrier can prevent the influx of pathogenic bacteria to induce inflammatory response. Overall, this study has deciphered, for the first time, the direct regulative effects of AhR activity on gut microbiota. Future research is warranted to elucidate the specific mechanisms of AhR action on certain bacterial population. Copyright © 2019 Elsevier Ltd. All rights reserved.
Original languageEnglish
Article number113357
JournalEnvironmental Pollution
Volume255
Issue numberPart 3
Early online dateOct 2019
DOIs
Publication statusPublished - Dec 2019

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Aryl Hydrocarbon Receptors
Dioxins
Zebrafish
Chemical activation
Hydrocarbons
Health
Bacteria
Dysbiosis
Inflammation
Legionella
Oxidative stress
Gastrointestinal Microbiome
Polychlorinated Biphenyls
Polychlorinated biphenyls
Fish
Intestines
Toxicity
Fishes
Oxidative Stress
Modulation

Citation

Sun, Y., Tang, L., Liu, Y., Hu, C., Zhou, B., Lam, P. K. S., . . . Chen, L. (2019). Activation of aryl hydrocarbon receptor by dioxin directly shifts gut microbiota in zebrafish. Environmental Pollution, 255(Part 3). Retrieved from https://doi.org/10.1016/j.envpol.2019.113357

Keywords

  • Gut microbiota
  • Aryl hydrocarbon receptor
  • PCB126
  • CH223191
  • Zebrafish intestinal health