Mechanistic insights of magnolol antimicrobial activity against Mycoplasma using untargeted metabolomic analyses

Hu Qiao; Zhang Tengfei; Zhang Wenting; Lu Qin; Guo Yunqing; Cao Xiaoyi; Shao Huabin; Zhai Xinguo; Luo Qingping

doi:10.3389/fcimb.2023.1325347

Mechanistic insights of magnolol antimicrobial activity against Mycoplasma using untargeted metabolomic analyses

Front Cell Infect Microbiol. 2023 Dec 12:13:1325347. doi: 10.3389/fcimb.2023.1325347. eCollection 2023.

Authors

Hu Qiao¹, Zhang Tengfei¹, Zhang Wenting¹, Lu Qin¹, Guo Yunqing¹, Cao Xiaoyi^{1

2}, Shao Huabin¹, Zhai Xinguo², Luo Qingping^{1

3}

Affiliations

¹ Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Hubei Provincial Key Laboratory of Animal Pathogenic Microbiology, Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan, China.
² College of Life Science and Food Engineering, Hebei University of Technology, Hebei, China.
³ Hubei Hongshan Laboratory, Wuhan, China.

Abstract

The unreasonable use of antibiotics is one of the important causes of antimicrobial resistance (AMR) that poses a huge public health threat. Magnolol is a traditional Chinese medicine exhibiting antibacterial-, antifungal-, anti-inflammatory-, and antioxidant activities. However, it is unclear whether magnolol has an inhibitory effect on mycoplasma. This study found that magnolol showed excellent inhibitory activity against various mycoplasmas. Magnolol showed dose-dependent inhibition of Mycoplasma synoviae growth and biofilm formation in vitro. Magnolol caused severely sunken and wrinkled M. synoviae cell membranes at the minimum inhibitory concentration, and an enlarged cell diameter. The chicken embryo infection model showed that magnolol significantly reduced M. synoviae pathogenicity in vivo. Kyoto Encyclopedia of Genes and Genomes pathway analysis showed that the citrate cycle, glycolysis/gluconeogenesis, and pyruvate metabolism were significantly disturbed at the minimum inhibitory concentration of magnolol. Interestingly, 41% of differential metabolites were in the categories of lipids and lipid-like molecules. Protegenin A was up-regulated 58752-fold after magnolol treatment. It belongs to fatty acyls, and destroys cell membrane integrity and cell activity. Ghosphatidylethanolamine, phosphatidylglycerol, phosphatidic acid, and phosphatidylserine related to membrane maintenance and stress response were widely down-regulated. Collectively, our results illustrate the feasibility of magnolol as a phytochemical compound to treat mycoplasma infection.

Keywords: Mycoplasma synoviae; biofilm; cell membrane; growth; lipid; magnolol; metabolomics; pathogenicity.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Anti-Bacterial Agents / pharmacology
Biphenyl Compounds / chemistry
Biphenyl Compounds / pharmacology
Chick Embryo
Lignans* / chemistry
Lignans* / pharmacology
Mycoplasma synoviae* / genetics

Substances

magnolol
Lignans
Anti-Bacterial Agents
Biphenyl Compounds

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the Postdoctoral Innovation Practice Posts in Hubei Province in 2022-2023 (No. 46), the National Natural Science Foundation of China (32202816), the National Key Research and Development Program of China (2022YFD1800602), the Key Research and Development Program of Hubei Province (2022BBA0055), the Industrial Chain Fund of Hongshan Laboratory (2022HSZD005),the Key Projects of Hubei Natural Science Foundation (2021CFA019) and the China Agriculture Research System (CARS-41).