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Monensin is an ionophore for monovalent cations, which is frequently used to prevent ketosis and to enhance performance in dairy cows. Studies have shown the rumen bacteria <i>Prevotella bryantii</i> B₁4 being less affected by monensin. The present study aimed to reveal more information about the respective molecular mechanisms in <i>P.</i><i>bryantii</i>, as there is still a lack of knowledge about defense mechanisms against monensin. Cell growth experiments applying increasing concentrations of monensin and incubations up to 72 h were done. Harvested cells were used for label-free quantitative proteomics, enzyme activity measurements, quantification of intracellular sodium and extracellular glucose concentrations and fluorescence microscopy. Our findings confirmed an active cell growth and fermentation activity of <i>P.</i><i>bryantii</i> B₁4 despite monensin concentrations up to 60 µM. An elevated abundance and activity of the Na⁺-translocating NADH:quinone oxidoreductase counteracted sodium influx caused by monensin. Cell membranes and extracellular polysaccharides were highly influenced by monensin indicated by a reduced number of outer membrane proteins, an increased number of certain glucoside hydrolases and an elevated concentration of extracellular glucose. Thus, a reconstruction of extracellular polysaccharides in <i>P.</i><i>bryantii</i> in response to monensin is proposed, which is expected to have a negative impact on the substrate binding capacities of this rumen bacterium.