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Lysyl-phosphatidylglycerol (L-PG) is one of the components of the mycobacterial membrane which contributes to the resistance towards cationic antimicrobial peptides, a host-induced frontline defense against invading pathogens. Its production is catalyzed by LysX, a bifunctional protein with lysyl transferase and lysyl-tRNA synthetase activity. Comparative proteome analysis of a lysX mutant of M. avium strain104 and the wild type indicated that the lysX mutant strain undergoes a transition in phenotype by switching the carbon metabolism to β-oxidation of fatty acids along with accumulation of lipid inclusions. Surprisingly, proteins associated with intracellular survival were upregulated in the lysX mutant even during the extracellular growth preparing the bacteria to the conditions occurring inside host cells. In line with this, the lysX mutant exhibited an enhanced intracellular growth in human blood-derived monocytes. Thus, our study exposes the significance of the gene lysX in the metabolism and virulence of the environmental pathogen, M. avium hominissuis.