myo-Inositol Catabolism in Bacillus subtilis

Abstract

The iolABCDEFGHIJ operon of Bacillus subtilis is responsible for myo-inositol catabolism involving multiple and stepwise reactions. Previous studies demonstrated that IolG and IolE are the enzymes for the first and second reactions, namely dehydrogenation of myo-inositol to give 2-keto-myo-inositol and the subsequent dehydration to 3D-(3,5/4)-trihydroxycyclohexane-1,2-dione. In the present studies the third reaction was shown to be the hydrolysis of 3D-(3,5/4)-trihydroxycyclohexane-1,2-dione catalyzed by IolD to yield 5-deoxy-D-glucuronic acid. The fourth reaction was the isomerization of 5-deoxy-D-glucuronic acid by IolB to produce 2-deoxy-5-keto-D-gluconic acid. Next, in the fifth reaction 2-deoxy-5-keto-D-gluconic acid was phosphorylated by IolC kinase to yield 2-deoxy-5-keto-D-gluconic acid 6-phosphate. IolR is known as the repressor controlling transcription of the iol operon. In this reaction 2-deoxy-5-keto-Dgluconic acid 6-phosphate appeared to be the intermediate acting as inducer by antagonizing DNA binding of IolR. Finally, IolJ turned out to be the specific aldolase for the sixth reaction, the cleavage of 2-deoxy-5-keto-D-gluconic acid 6-phosphate into dihydroxyacetone phosphate and malonic semialdehyde. The former is a known glycolytic intermediate, and the latter was previously shown to be converted to acetyl-CoA and CO 2 by a reaction catalyzed by IolA. The net result of the inositol catabolic pathway in B. subtilis is, thus, the conversion of myo-inositol to an equimolar mixture of dihydroxyacetone phosphate, acetyl-CoA, and CO 2 . myo-Inositol (MI)2 is abundant in soil and also common and essential in plants and animals. A number of microorganisms, including Bacillus subtilis (1), Cryptococcus melibiose (2), Aerobacter aerogenes (reclassified as Enterobacter aerogenes/Klebsiella mobilis) (3), Rhizobium leguminosarum bv. viciae (4), Sinorhizobium meliloti (5), Sinorhizobium fredii (6), Corynebacterium glutamicum (7), and Lactobacillus casei (8) can grow on MI as the sole carbon source. MI catabolism in A. aerogenes was studied biochemically, and a pathway of the catabolism finally yielding acetyl-CoA and dihydroxyacetone phosphate (DHAP) was proposed (9). However, our knowledge of the molecular genetics of bacterial MI catabolism has been restricted to B. subtilis (1, 10 -12). In B. subtilis, the iol divergon, comprising the operons iolABCDEFGHIJ and iolRS (1), and the iolT gene (12) were shown to be required for inositol catabolism (Fig. 1). Nowadays, a large number of bacteria have genes annotated iol in their genome sequence, but the annotation is only based on sequence similarity to B. subtilis iol genes, as relatively few studies have been done to demonstrate the participation of the deduced iol genes in MI catabolism.In B. subtilis, a repressor encoded by iolR is responsible for the regulation of all the iol genes (11, 12). In the absence of MI in the growth medium, the IolR repressor binds to the operator site within the promoter regions to repress the transcription. In its presence, howev...

Global Transcriptional Analysis of Virus-Host Interactions between Phage ϕ29 and Bacillus subtilis

“…The structure of the iol operon for myo-inositol catabolism in B. subtilis consists of 10 genes (iolA to iolJ). Once myo-inositol is incorporated into the cell, the inositol dehydrogenase encoded by iolG catalyzes its oxidation to 2-keto-myo-inositol, which is the first reaction of the catabolic pathway that results in the conversion of myo-inositol to an equimolar mixture of dihydroxyacetone phosphate, acetyl-CoA, and CO 2 (46,47). Glucose repression of the operon is exerted through catabolite repression mediated by CcpA and also by IolR.…”

An l-glucose Catabolic Pathway in Paracoccus Species 43P

“…Together, these results strongly indicate that the physiological role of LgdA involves scyllo-inositol catabolism. Among inositol dehydrogenases (IDHs), myo-IDH of Bacillus subtilis (IolG) is the best characterized enzyme, and it was reported to catalyze oxidation of the axial hydroxyl group of myo-inositol and D-chiro-inositol (22). IolG also catalyzes oxidation of ␣-D-glucose and ␣-D-xylose (23), which possess the same stereo-configuration of myo-inositol hydroxyl groups.…”

Carbon Catabolite Control of the Metabolic Network inBacillus subtilis

“…The operons involved in the catabolism of secondary carbon sources are as follows (the carbon sources in parentheses): gntRKPZ (gluconate), 16,35,36) xylAB (xylose), 9) iolABCDEFGHIJ (myo-inositol), 40,41,102) trePAR (trehalose), 25,47,103) galKT (galactose), 25) glpFK (glycerol), 33) glvARC (6-P--glucoside), 34) bglPH ( -glucoside), 26,27) yjlBCD-uxaC-yjmBCD-uxuA-yjmFexuTR-uxaBA (hexuronate), 25,48) xynPB ( -xyloside), 65) yxjC-scoAE-bdh ( -hydroxybutyrate), 25,49) ara-ABDLMNPQ-abfA (arabinose) 24,52,53) and abnA xsa (arabinose), 50) kdgRKAT (hexuronate), 25,42) and kduID (galacturonate). 43) The yxkF-msmX operon probably involved in the transport of unknown sugars has been found to be under CcpA-mediated CCR.…”