Identification of two scyllo-inositol dehydrogenases in Bacillus subtilis

Morinaga, Tetsuro; Ashida, Hitoshi; Yoshida, Ken-ichi

doi:10.1099/mic.0.037499-0

Cited by 39 publications

(64 citation statements)

References 33 publications

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“…It is interesting that myo-and especially scyllo-inositol serve as excellent carbon sources for S. meliloti, since the wild types grew to an OD 600 of Ͼ1 in minimal medium, which is comparable to growth with other C sources, such as glucose, glycerol, or succinate. This is in contrast to B. subtilis, which does not grow as efficiently with myoor scyllo-inositol as with glucose (25). Similarly, a lag time of 60 h has been reported for Salmonella enterica when grown with myo-inositol (19).…”

Section: Discussionmentioning

confidence: 62%

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Inositol Catabolism, a Key Pathway in Sinorhizobium meliloti for Competitive Host Nodulation

Kohler

Zheng

Schoffers

et al. 2010

Appl Environ Microbiol

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The nitrogen-fixing symbiont of alfalfa, Sinorhizobium meliloti, is able to use myo-inositol as the sole carbon source. Putative inositol catabolism genes (iolA and iolRCDEB) have been identified in the S. meliloti genome based on their similarities with the Bacillus subtilis iol genes. In this study, functional mutational analysis revealed that the iolA and iolCDEB genes are required for growth not only with the myo-isomer but also for growth with scyllo-and D-chiro-inositol as the sole carbon source. An additional, hypothetical dehydrogenase of the IdhA/MocA/GFO family encoded by the smc01163 gene was found to be essential for growth with scyllo-inositol, whereas the idhA-encoded myo-inositol dehydrogenase was responsible for the oxidation of D-chiro-inositol. The putative regulatory iolR gene, located upstream of iolCDEB, encodes a repressor of the iol genes, negatively regulating the activity of the myo-and the scyllo-inositol dehydrogenases. Mutants with insertions in the iolA, smc01163, and individual iolRCDE genes could not compete against the wild type in a nodule occupancy assay on alfalfa plants. Thus, a functional inositol catabolic pathway and its proper regulation are important nutritional or signaling factors in the S. meliloti-alfalfa symbiosis.The sugar alcohol inositol, or cyclohexanehexol, occurs in several different stereoisomers, of which the myo-form (Fig. 1, compound 1) is the most abundant (1). myo-Inositol plays important structural and signaling roles in animal and plant cells (22). In the environment, myo-inositol mainly occurs in the phosphorylated form and is involved in the phosphate cycle of terrestrial and freshwater ecosystems (41). The stereoisomers D-chiro-and scylloinositol have recently attracted attention, because they have shown therapeutic potentials for diabetes and Alzheimer's disease, respectively (11, 21). Although there is only limited knowledge about the metabolism of D-chiro-and scyllo-inositol (25, 50), the catabolism of myo-inositol has been studied in a variety of microorganisms, including some members of the Firmicutes (17, 46, 51), Enterobacteriaceae (4,19,40), and Rhizobiaceae (16,29). The myo-inositol catabolic pathway and its regulation are best understood in the Gram-positive bacterium Bacillus subtilis. The B. subtilis iol genes are organized in a divergon comprising iolABCDEFGHIJ and iolRS (47-49). In the proposed inositol catabolic pathway, the myo-inositol dehydrogenase oxidizes myoinositol to its corresponding ketone 2-keto-myo-inositol (2KMI), which is then further catabolized by the actions of IolE, -D, -B, -C, -J, and -A (Fig. 1). The inducer of the inositol catabolic pathway in B. subtilis is the product of the IolC reaction, 2-deoxy-5-keto-D-gluconic acid 6-phosphate (DKGP; compound 6 in Fig. 1), which antagonizes the binding of the IolR repressor to the iol promoter region (51).Sinorhizobium meliloti, the nitrogen-fixing symbiont of alfalfa, can use myo-inositol as the sole carbon source (15). The idhA-encoded myo-inositol dehydrogenase had been s...

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Section: Discussionmentioning

confidence: 62%

“…Recently, two scyllo-inositol dehydrogenases were identified in B. subtilis, IolX and IolW (25). Both purified enzymes reacted with scylloinositol, but only the iolX mutant showed impaired growth with scyllo-inositol as the sole C source (25).…”

Section: Discussionmentioning

confidence: 99%

Inositol Catabolism, a Key Pathway in Sinorhizobium meliloti for Competitive Host Nodulation

Kohler

Zheng

Schoffers

et al. 2010

Appl Environ Microbiol

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“…The deduced gene product of smc01163 displays an N-terminal signal peptide, suggesting a periplasmic location. So far, only two other scyllo-inositol dehydrogenases have been described from any organisms, namely, IolW and IolX in B. subtilis (25). IolW and IolX are probable cytoplasmic enzymes and share limited identity with Smc01163 (26 and 27%, respectively).…”

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confidence: 99%

The RpiR-Like Repressor IolR Regulates Inositol Catabolism in Sinorhizobium meliloti

2011

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Sinorhizobium meliloti, the nitrogen-fixing symbiont of alfalfa, has the ability to catabolize myo-, scyllo-, and D-chiro-inositol. Functional inositol catabolism (iol) genes are required for growth on these inositol isomers, and they play a role during plant-bacterium interactions. The inositol catabolism genes comprise the chromosomally encoded iolA (mmsA) and the iolY(smc01163)RCDEB genes, as well as the idhA gene located on the pSymB plasmid. Reverse transcriptase assays showed that the iolYRCDEB genes are transcribed as one operon. The iol genes were weakly expressed without induction, but their expression was strongly induced by myoinositol. The putative transcriptional regulator of the iol genes, IolR, belongs to the RpiR-like repressor family. Electrophoretic mobility shift assays demonstrated that IolR recognized a conserved palindromic sequence (5-GGAA-N 6 -TTCC-3) in the upstream regions of the idhA, iolY, iolR, and iolC genes. Complementation assays found IolR to be required for the repression of its own gene and for the downregulation of the idhA-encoded myo-inositol dehydrogenase activity in the presence and absence of inositol. Further expression studies indicated that the late pathway intermediate 2-keto-5-deoxy-D-gluconic acid 6-phosphate (KDGP) functions as the true inducer of the iol genes. The iolA (mmsA) gene encoding methylmalonate semialdehyde dehydrogenase was not regulated by IolR. The S. meliloti iolA (mmsA) gene product seems to be involved in more than only the inositol catabolic pathway, since it was also found to be essential for valine catabolism, supporting its more recent annotation as mmsA.

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“…B. subtilis possesses two additional inositol dehydrogenases, IolX and IolW, which act specifically on SI with NAD + and NADP + reduction, respectively, to convert it to scyllo-inosose. 4 In vivo and in vitro analyses have revealed that IolX plays the major physiological role in SI catabolism, whereas IolW efficiently reduces scylloinosose into SI with oxidation of NADPH. 4 scyllo-Inosose is metabolized sequentially in multiple steps involving the IolE, IolD, IolB, IolC, IolJ, and IolA enzymes to give common intermediates, dihydroxyacetone phosphate and acetylCoA, which enter glycolysis and the TCA cycle, respectively.…”

Section: Introductionmentioning

confidence: 99%

“…4 In vivo and in vitro analyses have revealed that IolX plays the major physiological role in SI catabolism, whereas IolW efficiently reduces scylloinosose into SI with oxidation of NADPH. 4 scyllo-Inosose is metabolized sequentially in multiple steps involving the IolE, IolD, IolB, IolC, IolJ, and IolA enzymes to give common intermediates, dihydroxyacetone phosphate and acetylCoA, which enter glycolysis and the TCA cycle, respectively. 5 We developed a B. subtilis cell factory to produce SI, where MI was chosen as a starting material that is abundant in nature and cheaply available from rice bran.…”

Section: Introductionmentioning

confidence: 99%

A second-generationBacilluscell factory for rare inositol production

Tanaka¹,

Takanaka²,

Yoshida³

2014

Bioengineered

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Landes Bioscience aDDeNDUM S ome rare inositol stereoisomers are known to exert specific healthpromoting effects, including scylloinositol (SI), which is a promising therapeutic agent for Alzheimer disease. We recently reported a Bacillus subtilis cell factory that performed the efficient production of SI from the cheapest and most abundant isomer myo-inositol (MI). In the cell factory all "useless" genes involved in MI and SI metabolism were deleted and overexpression of the key enzymes, IolG and IolW, was appended. It converted 10 g/L MI into the same amount of SI in 48 h of cultivation. In this addendum, we discuss further improvement in the cell factory and its possible applications.

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Identification of two scyllo-inositol dehydrogenases in Bacillus subtilis

Cited by 39 publications

References 33 publications

Inositol Catabolism, a Key Pathway in Sinorhizobium meliloti for Competitive Host Nodulation

Inositol Catabolism, a Key Pathway in Sinorhizobium meliloti for Competitive Host Nodulation

The RpiR-Like Repressor IolR Regulates Inositol Catabolism in Sinorhizobium meliloti

A second-generationBacilluscell factory for rare inositol production

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