| Summary: | (1) Background: Methicillin-resistant <i>Staphylococcus</i> <i>aureus</i> (MRSA) is a zoonotic pathogen that causes endocarditis, pneumonia, and skin diseases in humans and livestock. (2) Methods: The antibacterial effect of the total flavonoid against MRSA (ATCC43300) extracted from the <i>Agrimonia pilosa</i> Ledeb. (<i>A</i><i>. pilosa</i> Ledeb) was evaluated by the microdilution method. The oxidative stresses in MRSA were evaluated by the levels of intracellular hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), reactive oxygen species (ROS), and oxidative stress-related genes. The DNA oxidative damage was tested by the 8-hydroxy-2′-deoxyguanosine (8-OHdG) and DNA gel electrophoresis. The differentially expressed proteins were determined by the method of SDS-PAGE and NanoLC-ESI-MS/MS, while the mRNAs of differential proteins were determined by Real-Time PCR. The changes of ultra-structures in MRSA were observed by Transmission Electron Microscope (TEM). (3) Results: The minimum inhibitory concentration (MIC) of the total flavonoid against MRSA was recorded as 62.5 μg/mL. After treatment with the total flavonoid, the levels of intracellular H<sub>2</sub>O<sub>2</sub> and ROS were increased and the gene expressions against oxidative stress (<i>SodA</i>, <i>katA</i>, <i>TrxB</i>) were decreased (<i>p</i> < 0.01), while the gene expression for oxidative stress (<i>PerR</i>) was increased (<i>p</i> < 0.01). The level of intracellular 8-OHdG in MRSA was increased (<i>p</i> < 0.01) and the DNA was damaged. The results of TEM also showed that the total flavonoid could destroy the ultra-structures in the bacteria. (4) Conclusions: The total flavonoid extracted from the <i>A</i><i>. pilosa</i> Ledeb can induce the oxidative stress that disturbed the energy metabolism and protein synthesis in MRSA.
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