Newly Identified Nucleoid-Associated-Like Protein YlxR Regulates Metabolic Gene Expression in Bacillus subtilis

Glucose is the most favorable carbon source for the majority of bacteria, which have several glucose-responsive gene networks. Recently, we found that in Bacillus subtilis, glucose induces expression of the extracellular sigma factor genes sigX/M. To explore the factors affecting this phenomenon, we performed a transposon mutagenesis screen for mutants with no glucose induction (GI) of sigX-lacZ and identified ylxR. YlxR is widely conserved in eubacteria. Further analysis revealed that ylxR is induced by glucose addition. In vitro DNA-binding and cytological studies suggested that YlxR is a nucleoid-associated protein (NAP) in B. subtilis. In many cases, NAPs influence transcription, recombination, and genome stability. Thus, we performed transcriptome sequencing (RNA-Seq) analysis to evaluate the impact of ylxR disruption on the transcriptome in the presence of glucose and observed that YlxR has a profound impact on metabolic gene expression in addition to that of four sigma factor genes. The wide fluctuations of gene expression may result in abolition of GI of sigX/M in the ylxR disruptant. IMPORTANCE Expression of genes encoding NAPs is often temporally regulated. According to results from single-cell analysis, the ylxR gene is induced by glucose and expressed in a bistable mode. These characteristics have not previously been reported for NAP gene expression. Transcriptional profiling of the ylxR disruptant revealed a change in the expression levels of approximately 400 genes, including genes for synthesis of 12 amino acids and 4 nucleotides, in addition to the SigX/M regulons. Thus, YlxR is a critical regulator of glucose response in B. subtilis.