Physiological Response of <i>Corynebacterium glutamicum</i> to Indole
The aromatic heterocyclic compound indole is widely spread in nature. Due to its floral odor indole finds application in dairy, flavor, and fragrance products. Indole is an inter- and intracellular signaling molecule influencing cell division, sporulation, or virulence in some bacteria that synthesi...
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MDPI AG
2020-12-01
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| Seri Bilgileri: | Microorganisms |
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| Online Erişim: | https://www.mdpi.com/2076-2607/8/12/1945 |
| _version_ | 1827700573868130304 |
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| author | Tatjana Walter Kareen H. Veldmann Susanne Götker Tobias Busche Christian Rückert Arman Beyraghdar Kashkooli Jannik Paulus Katarina Cankar Volker F. Wendisch |
| author_facet | Tatjana Walter Kareen H. Veldmann Susanne Götker Tobias Busche Christian Rückert Arman Beyraghdar Kashkooli Jannik Paulus Katarina Cankar Volker F. Wendisch |
| author_sort | Tatjana Walter |
| collection | DOAJ |
| description | The aromatic heterocyclic compound indole is widely spread in nature. Due to its floral odor indole finds application in dairy, flavor, and fragrance products. Indole is an inter- and intracellular signaling molecule influencing cell division, sporulation, or virulence in some bacteria that synthesize it from tryptophan by tryptophanase. <i>Corynebacterium glutamicum</i> that is used for the industrial production of amino acids including tryptophan lacks tryptophanase. To test if indole is metabolized by <i>C. glutamicum</i> or has a regulatory role, the physiological response to indole by this bacterium was studied. As shown by RNAseq analysis, indole, which inhibited growth at low concentrations, increased expression of genes involved in the metabolism of iron, copper, and aromatic compounds. In part, this may be due to iron reduction as indole was shown to reduce Fe<sup>3+</sup> to Fe<sup>2+</sup> in the culture medium. Mutants with improved tolerance to indole were selected by adaptive laboratory evolution. Among the mutations identified by genome sequencing, mutations in three transcriptional regulator genes were demonstrated to be causal for increased indole tolerance. These code for the regulator of iron homeostasis DtxR, the regulator of oxidative stress response RosR, and the hitherto uncharacterized Cg3388. Gel mobility shift analysis revealed that Cg3388 binds to the intergenic region between its own gene and the <i>iolT2-rhcM2D2</i> operon encoding inositol uptake system IolT2, maleylacetate reductase, and catechol 1,2-dioxygenase. Increased RNA levels of <i>rhcM2</i> in a <i>cg3388</i> deletion strain indicated that Cg3388 acts as repressor. Indole, hydroquinone, and 1,2,4-trihydroxybenzene may function as inducers of the <i>iolT2-rhcM2D2</i> operon in vivo as they interfered with DNA binding of Cg3388 at physiological concentrations in vitro. Cg3388 was named IhtR. |
| first_indexed | 2024-03-10T14:15:00Z |
| format | Article |
| id | doaj.art-cc1cc57c33814d4e8b8b77f06c3bf270 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T14:15:00Z |
| publishDate | 2020-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-cc1cc57c33814d4e8b8b77f06c3bf2702023-11-20T23:54:04ZengMDPI AGMicroorganisms2076-26072020-12-01812194510.3390/microorganisms8121945Physiological Response of <i>Corynebacterium glutamicum</i> to IndoleTatjana Walter0Kareen H. Veldmann1Susanne Götker2Tobias Busche3Christian Rückert4Arman Beyraghdar Kashkooli5Jannik Paulus6Katarina Cankar7Volker F. Wendisch8Genetics of Prokaryotes, Faculty of Biology and CeBiTec, Bielefeld University, 33615 Bielefeld, GermanyGenetics of Prokaryotes, Faculty of Biology and CeBiTec, Bielefeld University, 33615 Bielefeld, GermanyGenetics of Prokaryotes, Faculty of Biology and CeBiTec, Bielefeld University, 33615 Bielefeld, GermanyCenter for Biotechnology, Bielefeld University, 33615 Bielefeld, GermanyCenter for Biotechnology, Bielefeld University, 33615 Bielefeld, GermanyBU Bioscience, Wageningen University & Research, 6700AA Wageningen, The NetherlandsOrganic and Bioorganic Chemistry, Department of Chemistry, Bielefeld University, 33615 Bielefeld, GermanyBU Bioscience, Wageningen University & Research, 6700AA Wageningen, The NetherlandsGenetics of Prokaryotes, Faculty of Biology and CeBiTec, Bielefeld University, 33615 Bielefeld, GermanyThe aromatic heterocyclic compound indole is widely spread in nature. Due to its floral odor indole finds application in dairy, flavor, and fragrance products. Indole is an inter- and intracellular signaling molecule influencing cell division, sporulation, or virulence in some bacteria that synthesize it from tryptophan by tryptophanase. <i>Corynebacterium glutamicum</i> that is used for the industrial production of amino acids including tryptophan lacks tryptophanase. To test if indole is metabolized by <i>C. glutamicum</i> or has a regulatory role, the physiological response to indole by this bacterium was studied. As shown by RNAseq analysis, indole, which inhibited growth at low concentrations, increased expression of genes involved in the metabolism of iron, copper, and aromatic compounds. In part, this may be due to iron reduction as indole was shown to reduce Fe<sup>3+</sup> to Fe<sup>2+</sup> in the culture medium. Mutants with improved tolerance to indole were selected by adaptive laboratory evolution. Among the mutations identified by genome sequencing, mutations in three transcriptional regulator genes were demonstrated to be causal for increased indole tolerance. These code for the regulator of iron homeostasis DtxR, the regulator of oxidative stress response RosR, and the hitherto uncharacterized Cg3388. Gel mobility shift analysis revealed that Cg3388 binds to the intergenic region between its own gene and the <i>iolT2-rhcM2D2</i> operon encoding inositol uptake system IolT2, maleylacetate reductase, and catechol 1,2-dioxygenase. Increased RNA levels of <i>rhcM2</i> in a <i>cg3388</i> deletion strain indicated that Cg3388 acts as repressor. Indole, hydroquinone, and 1,2,4-trihydroxybenzene may function as inducers of the <i>iolT2-rhcM2D2</i> operon in vivo as they interfered with DNA binding of Cg3388 at physiological concentrations in vitro. Cg3388 was named IhtR.https://www.mdpi.com/2076-2607/8/12/1945<i>Corynebacterium glutamicum</i>amino acidsindoleadaptive laboratory evolutioniron homeostasisoxidative stress |
| spellingShingle | Tatjana Walter Kareen H. Veldmann Susanne Götker Tobias Busche Christian Rückert Arman Beyraghdar Kashkooli Jannik Paulus Katarina Cankar Volker F. Wendisch Physiological Response of <i>Corynebacterium glutamicum</i> to Indole Microorganisms <i>Corynebacterium glutamicum</i> amino acids indole adaptive laboratory evolution iron homeostasis oxidative stress |
| title | Physiological Response of <i>Corynebacterium glutamicum</i> to Indole |
| title_full | Physiological Response of <i>Corynebacterium glutamicum</i> to Indole |
| title_fullStr | Physiological Response of <i>Corynebacterium glutamicum</i> to Indole |
| title_full_unstemmed | Physiological Response of <i>Corynebacterium glutamicum</i> to Indole |
| title_short | Physiological Response of <i>Corynebacterium glutamicum</i> to Indole |
| title_sort | physiological response of i corynebacterium glutamicum i to indole |
| topic | <i>Corynebacterium glutamicum</i> amino acids indole adaptive laboratory evolution iron homeostasis oxidative stress |
| url | https://www.mdpi.com/2076-2607/8/12/1945 |
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