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Mycobacterium smegmatis  ( Msm ), along with its pathogenic counterpart  Mycobacterium tuberculosis  ( Mtb ), utilizes fatty acids and cholesterol as important carbon and energy sources during the persistence within host cells. As a dual-functional enzyme in the glyoxylate cycle and the methylcitrate cycle, isocitrate lyase (ICL, encoded by  icl  or  MSMEG_0911 ) is indispensable for the growth of  Msm  and  Mtb  on short-chain fatty acids. However, regulation of  icl  in mycobacteria in response to nutrient availability remains largely unknown. Here, we report that the global nitrogen metabolism regulator GlnR represses  icl  expression by binding to an atypical binding motif in the  icl  promoter region under nitrogen-limiting conditions. We further show that GlnR competes with PrpR, a transcriptional activator of  icl , and dominantly occupies the co-binding motif in the  icl  promoter region. In the absence of GlnR or in response to the excess nitrogen condition,  Msm  cells elongate and exhibit robust growth on short-chain fatty acids due to the PrpR-mediated activation of  icl , thereby inducing enhanced apoptosis in infected macrophages. Taken together, our findings reveal the GlnR-mediated repression of  icl  on fatty acid metabolism, which might be a general strategy of nutrient sensing and environmental adaptation employed by mycobacteria.

Mycobacterium smegmatis GlnR Regulates the Glyoxylate Cycle and the Methylcitrate Cycle on Fatty Acid Metabolism by Repressing icl Transcription