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, 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.
Highlights
Cinnamic acid, an aromatic compound with a distinct aroma, is naturally found as a free compound in several plants, such as Cinnamomum verum, C. cassia, and C. zeylanicum (He et al, 2005; Gruenwald et al, 2010)
cinnamic acid decarboxylase (CdcA), sorbic acid decarboxylase regulator (SdrA), and PadA Are Essential for Cinnamic Acid and Sorbic Acid Utilization
To understand the role of CdcA (NRRL3_8296), SdrA (NRRL3_8297), and PadA (NRRL3_8298) for aromatic metabolism in A. niger, deletion mutants were made and tested on a set of related aromatic compounds as a sole carbon source. cdcA and padA resulted in abolished growth on cinnamic acid and reduced growth on sorbic acid, while deletion of sdrA resulted in reduced growth on both cinnamic acid and sorbic acid
Summary
An aromatic compound with a distinct aroma, is naturally found as a free compound in several plants, such as Cinnamomum verum, C. cassia, and C. zeylanicum (He et al, 2005; Gruenwald et al, 2010). Two genes were identified in Aspergillus niger and Saccharomyces cerevisiae, that are involved in the non-oxidative decarboxylation of cinnamic acid using prenylated flavin mononucleotide (FMN) as a cofactor to convert cinnamic acid to styrene (Plumridge et al, 2010; Payne et al, 2015). These genes are clustered in the genome and encode a putative 3-octaprenyl-4-hydroxybenzoate carboxylyase, referred to as cinnamic acid decarboxylase (cdcA, formerly ferulic acid decarboxylase (fdcA), see Discussion), and a flavin prenyltransferase (padA) (Figure 1) (Plumridge et al, 2010; Payne et al, 2015). Better understanding of the cinnamic acid metabolic pathway in A. niger can aid in the creation of cell factories or unlock new strategies to make valuable aromatic building blocks
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