Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus niger
Tannic acid, a hydrolysable gallotannin present in plant tissues, consists of a central glucose molecule esterified with gallic acid molecules. Some microorganisms, including several Aspergillus species, can metabolize tannic acid by releasing gallic acid residues from tannic acid by secreting tanni...
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Frontiers Media S.A.
2021-05-01
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| Series: | Frontiers in Fungal Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/ffunb.2021.681631/full |
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| author | Mark Arentshorst Marcos Di Falco Marie-Claude Moisan Ian D. Reid Tessa O. M. Spaapen Jisca van Dam Ebru Demirci Justin Powlowski Peter J. Punt Peter J. Punt Adrian Tsang Arthur F. J. Ram |
| author_facet | Mark Arentshorst Marcos Di Falco Marie-Claude Moisan Ian D. Reid Tessa O. M. Spaapen Jisca van Dam Ebru Demirci Justin Powlowski Peter J. Punt Peter J. Punt Adrian Tsang Arthur F. J. Ram |
| author_sort | Mark Arentshorst |
| collection | DOAJ |
| description | Tannic acid, a hydrolysable gallotannin present in plant tissues, consists of a central glucose molecule esterified with gallic acid molecules. Some microorganisms, including several Aspergillus species, can metabolize tannic acid by releasing gallic acid residues from tannic acid by secreting tannic acid specific esterases into the medium. The expression of these so-called tannases is induced by tannic acid or gallic acid. In this study, we identified a conserved transcriptional activator-repressor module involved in the regulation of predicted tannases and other genes involved in gallic acid metabolism. The transcriptional activator-repressor module regulating tannic acid utilization resembles the transcriptional activator-repressor modules regulating galacturonic acid and quinic acid utilization. Like these modules, the Zn(II)2Cys6 transcriptional activator (TanR) and the putative repressor (TanX) are located adjacent to each other. Deletion of the transcriptional activator (ΔtanR) results in inability to grow on gallic acid and severely reduces growth on tannic acid. Deletion of the putative repressor gene (ΔtanX) results in the constitutive expression of tannases as well as other genes with mostly unknown function. Known microbial catabolic pathways for gallic acid utilization involve so-called ring cleavage enzymes, and two of these ring cleavage enzymes show increased expression in the ΔtanX mutant. However, deletion of these two genes, and even deletion of all 17 genes encoding potential ring cleavage enzymes, did not result in a gallic acid non-utilizing phenotype. Therefore, in A. niger gallic acid utilization involves a hitherto unknown pathway. Transcriptome analysis of the ΔtanX mutant identified several genes and gene clusters that were significantly induced compared to the parental strain. The involvement of a selection of these genes and gene clusters in gallic acid utilization was examined by constructing gene deletion mutants and testing their ability to grow on gallic acid. Only the deletion of a gene encoding an FAD-dependent monooxygenase (NRRL3_04659) resulted in a strain that was unable to grow on gallic acid. Metabolomic studies showed accumulation of gallic acid in the ΔNRRL3_04659 mutant suggesting that this predicted monooxygenase is involved in the first step of gallic acid metabolism and is likely responsible for oxidation of the aromatic ring. |
| first_indexed | 2024-12-16T14:21:47Z |
| format | Article |
| id | doaj.art-e2f90148196547de96f3aeade63e0ad3 |
| institution | Directory Open Access Journal |
| issn | 2673-6128 |
| language | English |
| last_indexed | 2024-12-16T14:21:47Z |
| publishDate | 2021-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Fungal Biology |
| spelling | doaj.art-e2f90148196547de96f3aeade63e0ad32022-12-21T22:28:28ZengFrontiers Media S.A.Frontiers in Fungal Biology2673-61282021-05-01210.3389/ffunb.2021.681631681631Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus nigerMark Arentshorst0Marcos Di Falco1Marie-Claude Moisan2Ian D. Reid3Tessa O. M. Spaapen4Jisca van Dam5Ebru Demirci6Justin Powlowski7Peter J. Punt8Peter J. Punt9Adrian Tsang10Arthur F. J. Ram11Molecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, NetherlandsCentre for Structural and Functional Genomics, Concordia University, Montreal, QC, CanadaCentre for Structural and Functional Genomics, Concordia University, Montreal, QC, CanadaCentre for Structural and Functional Genomics, Concordia University, Montreal, QC, CanadaMolecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, NetherlandsMolecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, NetherlandsMolecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, NetherlandsDepartment of Chemistry & Biochemistry, Concordia University, Montreal, QC, CanadaMolecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, NetherlandsDutch DNA Biotech, Hugo R Kruytgebouw 4-Noord, Utrecht, NetherlandsCentre for Structural and Functional Genomics, Concordia University, Montreal, QC, CanadaMolecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, NetherlandsTannic acid, a hydrolysable gallotannin present in plant tissues, consists of a central glucose molecule esterified with gallic acid molecules. Some microorganisms, including several Aspergillus species, can metabolize tannic acid by releasing gallic acid residues from tannic acid by secreting tannic acid specific esterases into the medium. The expression of these so-called tannases is induced by tannic acid or gallic acid. In this study, we identified a conserved transcriptional activator-repressor module involved in the regulation of predicted tannases and other genes involved in gallic acid metabolism. The transcriptional activator-repressor module regulating tannic acid utilization resembles the transcriptional activator-repressor modules regulating galacturonic acid and quinic acid utilization. Like these modules, the Zn(II)2Cys6 transcriptional activator (TanR) and the putative repressor (TanX) are located adjacent to each other. Deletion of the transcriptional activator (ΔtanR) results in inability to grow on gallic acid and severely reduces growth on tannic acid. Deletion of the putative repressor gene (ΔtanX) results in the constitutive expression of tannases as well as other genes with mostly unknown function. Known microbial catabolic pathways for gallic acid utilization involve so-called ring cleavage enzymes, and two of these ring cleavage enzymes show increased expression in the ΔtanX mutant. However, deletion of these two genes, and even deletion of all 17 genes encoding potential ring cleavage enzymes, did not result in a gallic acid non-utilizing phenotype. Therefore, in A. niger gallic acid utilization involves a hitherto unknown pathway. Transcriptome analysis of the ΔtanX mutant identified several genes and gene clusters that were significantly induced compared to the parental strain. The involvement of a selection of these genes and gene clusters in gallic acid utilization was examined by constructing gene deletion mutants and testing their ability to grow on gallic acid. Only the deletion of a gene encoding an FAD-dependent monooxygenase (NRRL3_04659) resulted in a strain that was unable to grow on gallic acid. Metabolomic studies showed accumulation of gallic acid in the ΔNRRL3_04659 mutant suggesting that this predicted monooxygenase is involved in the first step of gallic acid metabolism and is likely responsible for oxidation of the aromatic ring.https://www.frontiersin.org/articles/10.3389/ffunb.2021.681631/fullring cleavage enzymetannasesmonooxygenaseZn(II)2Cys6 transcriptional activatorgene regulationring cleaving enzymes |
| spellingShingle | Mark Arentshorst Marcos Di Falco Marie-Claude Moisan Ian D. Reid Tessa O. M. Spaapen Jisca van Dam Ebru Demirci Justin Powlowski Peter J. Punt Peter J. Punt Adrian Tsang Arthur F. J. Ram Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus niger Frontiers in Fungal Biology ring cleavage enzyme tannases monooxygenase Zn(II)2Cys6 transcriptional activator gene regulation ring cleaving enzymes |
| title | Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus niger |
| title_full | Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus niger |
| title_fullStr | Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus niger |
| title_full_unstemmed | Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus niger |
| title_short | Identification of a Conserved Transcriptional Activator-Repressor Module Controlling the Expression of Genes Involved in Tannic Acid Degradation and Gallic Acid Utilization in Aspergillus niger |
| title_sort | identification of a conserved transcriptional activator repressor module controlling the expression of genes involved in tannic acid degradation and gallic acid utilization in aspergillus niger |
| topic | ring cleavage enzyme tannases monooxygenase Zn(II)2Cys6 transcriptional activator gene regulation ring cleaving enzymes |
| url | https://www.frontiersin.org/articles/10.3389/ffunb.2021.681631/full |
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