Systematic metadata analysis of brown rot fungi gene expression data reveals the genes involved in Fenton's reaction and wood decay process

Abstract

Brown-rot fungi are rapid holocellulose degraders and are the most predominant degraders of coniferous wood products in North America. Brown-rot fungi degrades wood by both enzymatic (plant biomass degrading carbohydrate active enzymes-CAZymes) and non-enzymatic systems (Fenton's reaction) mechanisms. Identifying the genes and molecular mechanisms involved in Fenton's reaction would significantly improve our understanding about brown-rot decay. Our present study identifies the common gene expression patterns involved in brown rot decay by performing metadata analysis of fungal transcriptome datasets. We have also analyzed and compared the genome-wide annotations (InterPro and CAZymes) of the selected brown rot fungi. Genes encoding for various oxidoreductases, iron homeostasis, and metabolic enzymes involved in Fenton's mechanism were found to be significantly expressed among all the brown-rot fungal datasets. Interestingly, a higher number of hemicellulases encoding genes were differentially expressed among all the datasets, while a fewer number of cellulases and peroxidases were expressed (especially haem peroxidase and chloroperoxidase). Apart from these lignocellulose degrading enzymes genes encoding for aldo/keto reductases, 2-nitro dioxygenase, aromatic-ring dioxygenase, dienelactone hydrolase, alcohol dehydrogenase, major facilitator superfamily, cytochrome-P450 monoxygenase, cytochrome b5, and short-chain dehydrogenase were common and differentially up regulated among all the analyzed brown-rot fungal datasets.

Keywords: Fenton’s reaction; Haber-Weiss reaction; Plant biomass; brown-rot fungi; lignocellulose; wood-decaying fungi.

Graphical abstract

Figure 1.

Time scale panel generated by the TimeTree-the time scale of life web-database. The time scale panel displays the divergence of geological time scale, earth impacts, levels of oxygen, carbon dioxide and solar luminosity. Time divergence between all the selected taxa except for F. radiculosa is displayed above the time scale panel.

Figure 2.

Pictorial representation of genome wide distribution genes encoding for hydrogenosomal/mitochondrial iron uptake and metabolism, [Note: P.pl = Rhodonia placenta, W.co = Wolfiporia cocos, C.pu = Coniophora puteana, H.pi = Hydnomerulius pinastri, S.la = Serpula lacrymans and F.ra = Fibroporia radiculosa] .

Figure 3.

(a) Violin plots showing the distribution of differentially expressed significant genes in GSE12540, GSE29656, GSE69012, and GSE84529 datasets. Venn diagrams showing the number of commonly expressed genes among the R. placenta datasets (b) Venn diagram of differentially expressed significant genes among the GSE12540-GSE29656 datasets experimental conditions where BMA- Ball milled aspen, BMP-Ball milled pine, GLU- glucose, CEL-Cellulose. (c) Venn diagram of differentially expressed significant genes among the experimental conditions of GSE69012 dataset where A- high lignin: low glucose, B- low lignin: high glucose, C- average lignin: average glucose, ABC-10, ABC-20 and ABC-30 refers to genes common among A,B and C datasets cultured at 10, 20 and 30 days of incubation periods, (d) Venn diagram of differentially expressed significant genes among the experimental conditions of GSE84529 dataset where 0-5mm vs 15-20mm, here we have compared the differentially expressed gene list obtained from 0-5mm vs 15-20mm growth conditions similar for other compared conditions 30-35mm vs 0-5mm and 30-35mm vs 15-20mm respectively.

Figure 4.

(a) Violin plots showing the distribution of differentially expressed significant genes obtained in GSE78007 dataset, (b) Six-way Venn diagram showing the number of commonly expressed genes among the experimental conditions of GSE78007 dataset, (c) Three-way Venn diagram showing the number of common differentially expressed significant genes among the H. pinastri, S. lacrymans, C. puteana in GSE64897 dataset.

Figure 5.

Six-way Venn diagrams showing the number of commonly expressed genes among the (a) genome wide proteomic annotations and (b) differentially expressed significant genes from the gene expression datasets.

Figure 6.

Pictorial representation of genome-wide CAZymes (a) genome wide distribution of CAZymes among all the selected brown rot fungi. (b) ligninolytic- auxiliary activity (AA), (c) pectinolytic, (d) cellulolytic, (e) hemicellulolytic, (f) tentative distribution of genes encoding for lignocellulolytic CAZymes in Rhodonia placenta (P. p), Fibroporia radiculosa (F. r), Wolfiporia cocos (W. c), Coniophora puteana (C. p), Serpula lacrymans (S. l), Hydnomerulius pinastri (H. p). [Note: Figure 5(a): AA = Auxiliary Activity, CBM = Carbohydrate binding modules, CE = Carbohydrate esterases, EXPN = Expansins, GH = Glycoside hydrolases, PL = Polysaccharide lyases and CAZY = Total number of carbohydrate active enzymes] .

Figure 7.

Pictorial representation of brown-rot fungal Fenton’s reaction mechanism differentiating the reaction mechanism in plant wood cell lumen and plant wood cell wall.