Cinnamic Acid and Sorbic acid Conversion Are Mediated by the Same Transcriptional Regulator in Aspergillus niger

doi:10.3389/fbioe.2019.00249

Title: Cinnamic Acid and Sorbic acid Conversion Are Mediated by the Same Transcriptional Regulator in Aspergillus niger

Abstract

Cinnamic acid is an aromatic compound commonly found in plants and functions as a central intermediate in lignin synthesis. Filamentous fungi are able to degrade cinnamic acid through multiple metabolic pathways. One of the best studied pathways is the non-oxidative decarboxylation of cinnamic acid to styrene. In Aspergillus niger, the enzymes cinnamic acid decarboxylase (CdcA, formally ferulic acid decarboxylase) and the flavin prenyltransferase (PadA) catalyze together the non-oxidative decarboxylation of cinnamic acid and sorbic acid. The corresponding genes, cdcA and padA, are clustered in the genome together with a putative transcription factor previously named sorbic acid decarboxylase regulator (SdrA). While SdrA was predicted to be involved in the regulation of the non-oxidative decarboxylation of cinnamic acid and sorbic acid, this was never functionally analyzed. In this study, A. niger deletion mutants of sdrA, cdcA, and padA were made to further investigate the role of SdrA in cinnamic acid metabolism. Phenotypic analysis revealed that cdcA, sdrA and padA are exclusively involved in the degradation of cinnamic acid and sorbic acid and not required for other related aromatic compounds. Whole genome transcriptome analysis of ΔsdrA grown on different cinnamic acid related compounds, revealed additional target genes, which were also clustered with cdcA,more »« less

Authors:: Lubbers, Ronnie J. M.; Dilokpimol, Adiphol; Navarro, Jorge; Peng, Mao; Wang, Mei; Lipzen, Anna; Ng, Vivian; Grigoriev, Igor V.; Visser, Jaap; Hildén, Kristiina S.; de Vries, Ronald P.

Publication Date:: 2019-09-27

Research Org.:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC)

OSTI Identifier:: 1566916

Alternate Identifier(s):: OSTI ID: 1581323

Grant/Contract Number:: AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Frontiers in Bioengineering and Biotechnology

Additional Journal Information:: Journal Name: Frontiers in Bioengineering and Biotechnology Journal Volume: 7; Journal ID: ISSN 2296-4185

Publisher:: Frontiers Research Foundation

Country of Publication:: Switzerland

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; fungal aromatic metabolism; Aspergilli; synteny analysis; transcription factor; flavoprotein; cinnamic acid decarboxylase

Citation Formats


                    Lubbers, Ronnie J. M., Dilokpimol, Adiphol, Navarro, Jorge, Peng, Mao, Wang, Mei, Lipzen, Anna, Ng, Vivian, Grigoriev, Igor V., Visser, Jaap, Hildén, Kristiina S., and de Vries, Ronald P. Cinnamic Acid and Sorbic acid Conversion Are Mediated by the Same Transcriptional Regulator in Aspergillus niger.  Switzerland: N. p., 2019. 
        Web.  doi:10.3389/fbioe.2019.00249.

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                    Lubbers, Ronnie J. M., Dilokpimol, Adiphol, Navarro, Jorge, Peng, Mao, Wang, Mei, Lipzen, Anna, Ng, Vivian, Grigoriev, Igor V., Visser, Jaap, Hildén, Kristiina S., & de Vries, Ronald P. Cinnamic Acid and Sorbic acid Conversion Are Mediated by the Same Transcriptional Regulator in Aspergillus niger.  Switzerland.  doi:10.3389/fbioe.2019.00249.

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                    Lubbers, Ronnie J. M., Dilokpimol, Adiphol, Navarro, Jorge, Peng, Mao, Wang, Mei, Lipzen, Anna, Ng, Vivian, Grigoriev, Igor V., Visser, Jaap, Hildén, Kristiina S., and de Vries, Ronald P. Fri .  
        "Cinnamic Acid and Sorbic acid Conversion Are Mediated by the Same Transcriptional Regulator in Aspergillus niger".  Switzerland.  doi:10.3389/fbioe.2019.00249.

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@article{osti_1566916,

  title        = {Cinnamic Acid and Sorbic acid Conversion Are Mediated by the Same Transcriptional Regulator in Aspergillus niger},

  author       = {Lubbers, Ronnie J. M. and Dilokpimol, Adiphol and Navarro, Jorge and Peng, Mao and Wang, Mei and Lipzen, Anna and Ng, Vivian and Grigoriev, Igor V. and Visser, Jaap and Hildén, Kristiina S. and de Vries, Ronald P.},

  abstractNote = {Cinnamic acid is an aromatic compound commonly found in plants and functions as a central intermediate in lignin synthesis. Filamentous fungi are able to degrade cinnamic acid through multiple metabolic pathways. One of the best studied pathways is the non-oxidative decarboxylation of cinnamic acid to styrene. In Aspergillus niger, the enzymes cinnamic acid decarboxylase (CdcA, formally ferulic acid decarboxylase) and the flavin prenyltransferase (PadA) catalyze together the non-oxidative decarboxylation of cinnamic acid and sorbic acid. The corresponding genes, cdcA and padA, are clustered in the genome together with a putative transcription factor previously named sorbic acid decarboxylase regulator (SdrA). While SdrA was predicted to be involved in the regulation of the non-oxidative decarboxylation of cinnamic acid and sorbic acid, this was never functionally analyzed. In this study, A. niger deletion mutants of sdrA, cdcA, and padA were made to further investigate the role of SdrA in cinnamic acid metabolism. Phenotypic analysis revealed that cdcA, sdrA and padA are exclusively involved in the degradation of cinnamic acid and sorbic acid and not required for other related aromatic compounds. Whole genome transcriptome analysis of ΔsdrA grown on different cinnamic acid related compounds, revealed additional target genes, which were also clustered with cdcA, sdrA, and padA in the A. niger genome. Synteny analysis using 30 Aspergillus genomes demonstrated a conserved cinnamic acid decarboxylation gene cluster in most Aspergilli of the Nigri clade. Aspergilli lacking certain genes in the cluster were unable to grow on cinnamic acid, but could still grow on related aromatic compounds, confirming the specific role of these three genes for cinnamic acid metabolism of A. niger.},

  doi          = {10.3389/fbioe.2019.00249},

  journal      = {Frontiers in Bioengineering and Biotechnology},

  number       = ,

  volume       = 7,

  place        = {Switzerland},

  year         = {2019},

  month        = {9}

}

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Title: Cinnamic Acid and Sorbic acid Conversion Are Mediated by the Same Transcriptional Regulator in Aspergillus niger

Abstract

Citation Formats

Overexpression of PAD1 and FDC1 results in significant cinnamic acid decarboxylase activity in Saccharomyces cerevisiae journal, February 2015

Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli journal, January 1987

The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. journal, October 1994

Growth and Inhibition of Microorganisms in the Presence of Sorbic Acid: A Review journal, April 1985

The Catenin p120 ctn Interacts with Kaiso, a Novel BTB/POZ Domain Zinc Finger Transcription Factor journal, May 1999

Degradation of Potassium Sorbate by Penicillium Species journal, October 1966

The occurrence, metabolism and toxicity of cinnamic acid and related compounds journal, December 1984

The old 3-oxoadipate pathway revisited: New insights in the catabolism of aromatics in the saprophytic fungus Aspergillus nidulans journal, January 2015

The Aspergillus Genome Database (AspGD): recent developments in comprehensive multispecies curation, comparative genomics and community resources journal, November 2011

A comparison between the homocyclic aromatic metabolic pathways from plant-derived compounds by bacteria and fungi journal, November 2019

Mapping the structural requirements of inducers and substrates for decarboxylation of weak acid preservatives by the food spoilage mould Aspergillus niger journal, July 2012

Metabolism of cinnamic acid by Aspergillus niger journal, March 1969

Creating pathways towards aromatic building blocks and fine chemicals journal, December 2015

New cofactor supports α,β-unsaturated acid decarboxylation via 1,3-dipolar cycloaddition journal, June 2015

The decarboxylation of the weak-acid preservative, sorbic acid, is encoded by linked genes in Aspergillus spp. journal, August 2010

Metabolic Engineering of the Shikimate Pathway for Production of Aromatics and Derived Compounds—Present and Future Strain Construction Strategies journal, March 2018

Metabolic engineering for plant natural product biosynthesis in microbes journal, December 2008

Natural Formation of Styrene by Cinnamon Mold Flora journal, August 2009

Terminal Alkenes from Acrylic Acid Derivatives via Non-Oxidative Enzymatic Decarboxylation by Ferulic Acid Decarboxylases journal, July 2018

Combinatorial control of gene expression in Aspergillus niger grown on sugar beet pectin journal, September 2017

Isolation and molecular characterisation of the benzoate-para-hydroxylase gene (bphA) of Aspergillus niger: A member of a new gene family of the cytochrome P450 superfamily journal, September 1990

The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds journal, April 2002

Production in food of 1,3-pentadiene and styrene by Trichoderma species journal, May 2007

Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae journal, December 2005

Genomic Islands in the Pathogenic Filamentous Fungus Aspergillus fumigatus journal, April 2008

Genome sequencing and analysis of Aspergillus oryzae journal, December 2005

DeepLoc: prediction of protein subcellular localization using deep learning journal, July 2017

PAD1 and FDC1 are essential for the decarboxylation of phenylacrylic acids in Saccharomyces cerevisiae journal, June 2010

Metabolism of lignin related aromatic compounds by Aspergillus japonicus journal, January 1983

Authentication and Quantitative Analysis on the Chemical Profile of Cassia Bark (Cortex Cinnamomi) by High-Pressure Liquid Chromatography journal, April 2005

Production of Cinnamic and p-Hydroxycinnamic Acids in Engineered Microbes journal, August 2015

Fungal metabolism—I.The transformations of coumarin, o-coumaric acid and trans-cinnamic acid by Aspergillus niger journal, January 1967

The gold-standard genome of Aspergillus niger NRRL 3 enables a detailed view of the diversity of sugar catabolism in fungi journal, September 2018

Degradation of styrene by white-rot fungi journal, February 1997

Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus journal, February 2017

Cinnamon and Health journal, September 2010

Characterization and induction of phenolic acid decarboxylase from Aspergillus luchuensis journal, August 2018

Whole genome comparison of Aspergillus flavus and A. oryzae journal, January 2006

Highly efficient gene targeting in the Aspergillus niger kusA mutant journal, March 2007

Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger journal, November 1988

A New Black Aspergillus Species, A. vadensis, Is a Promising Host for Homologous and Heterologous Protein Production journal, July 2004

MycoCosm portal: gearing up for 1000 fungal genomes journal, December 2013

Biodegradation of a model allelochemical cinnamic acid by a novel endophytic fungus Phomopsis liquidambari journal, October 2015

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal, December 2014

Regulators of plant biomass degradation in ascomycetous fungi journal, June 2017

Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus journal, December 2005

Overexpression of PAD1 and FDC1 results in significant cinnamic acid decarboxylase activity in Saccharomyces cerevisiae
journal, February 2015

Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli
journal, January 1987

The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila.
journal, October 1994

Growth and Inhibition of Microorganisms in the Presence of Sorbic Acid: A Review
journal, April 1985

The Catenin p120 ^ctn Interacts with Kaiso, a Novel BTB/POZ Domain Zinc Finger Transcription Factor
journal, May 1999

Degradation of Potassium Sorbate by Penicillium Species
journal, October 1966

The occurrence, metabolism and toxicity of cinnamic acid and related compounds
journal, December 1984

The old 3-oxoadipate pathway revisited: New insights in the catabolism of aromatics in the saprophytic fungus Aspergillus nidulans
journal, January 2015

The Aspergillus Genome Database (AspGD): recent developments in comprehensive multispecies curation, comparative genomics and community resources
journal, November 2011

A comparison between the homocyclic aromatic metabolic pathways from plant-derived compounds by bacteria and fungi
journal, November 2019

Mapping the structural requirements of inducers and substrates for decarboxylation of weak acid preservatives by the food spoilage mould Aspergillus niger
journal, July 2012

Metabolism of cinnamic acid by Aspergillus niger
journal, March 1969

Creating pathways towards aromatic building blocks and fine chemicals
journal, December 2015

New cofactor supports α,β-unsaturated acid decarboxylation via 1,3-dipolar cycloaddition
journal, June 2015

The decarboxylation of the weak-acid preservative, sorbic acid, is encoded by linked genes in Aspergillus spp.
journal, August 2010

Metabolic Engineering of the Shikimate Pathway for Production of Aromatics and Derived Compounds—Present and Future Strain Construction Strategies
journal, March 2018

Metabolic engineering for plant natural product biosynthesis in microbes
journal, December 2008

Natural Formation of Styrene by Cinnamon Mold Flora
journal, August 2009

Terminal Alkenes from Acrylic Acid Derivatives via Non-Oxidative Enzymatic Decarboxylation by Ferulic Acid Decarboxylases
journal, July 2018

Combinatorial control of gene expression in Aspergillus niger grown on sugar beet pectin
journal, September 2017

Isolation and molecular characterisation of the benzoate-para-hydroxylase gene (bphA) of Aspergillus niger: A member of a new gene family of the cytochrome P450 superfamily
journal, September 1990

The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds
journal, April 2002

Production in food of 1,3-pentadiene and styrene by Trichoderma species
journal, May 2007

Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae
journal, December 2005

Genomic Islands in the Pathogenic Filamentous Fungus Aspergillus fumigatus
journal, April 2008

Genome sequencing and analysis of Aspergillus oryzae
journal, December 2005

DeepLoc: prediction of protein subcellular localization using deep learning
journal, July 2017

PAD1 and FDC1 are essential for the decarboxylation of phenylacrylic acids in Saccharomyces cerevisiae
journal, June 2010

Metabolism of lignin related aromatic compounds by Aspergillus japonicus
journal, January 1983

Authentication and Quantitative Analysis on the Chemical Profile of Cassia Bark (Cortex Cinnamomi) by High-Pressure Liquid Chromatography
journal, April 2005

Production of Cinnamic and p-Hydroxycinnamic Acids in Engineered Microbes
journal, August 2015

Fungal metabolism—I.The transformations of coumarin, o-coumaric acid and trans-cinnamic acid by Aspergillus niger
journal, January 1967

The gold-standard genome of Aspergillus niger NRRL 3 enables a detailed view of the diversity of sugar catabolism in fungi
journal, September 2018

Degradation of styrene by white-rot fungi
journal, February 1997

Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus
journal, February 2017

Cinnamon and Health
journal, September 2010

Characterization and induction of phenolic acid decarboxylase from Aspergillus luchuensis
journal, August 2018

Whole genome comparison of Aspergillus flavus and A. oryzae
journal, January 2006

Highly efficient gene targeting in the Aspergillus niger kusA mutant
journal, March 2007

Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger
journal, November 1988

A New Black Aspergillus Species, A. vadensis, Is a Promising Host for Homologous and Heterologous Protein Production
journal, July 2004

MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013

Biodegradation of a model allelochemical cinnamic acid by a novel endophytic fungus Phomopsis liquidambari
journal, October 2015

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014

Regulators of plant biomass degradation in ascomycetous fungi
journal, June 2017

Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus
journal, December 2005